Laboratory Primate Newsletter

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LABORATORY PRIMATE NEWSLETTER

Vol. 50, No. 1 January 2011

JUDITH E. SCHRIER, EDITOR JAMES S. HARPER, GORDON J. HANKINSON AND LARRY HULSEBOS, ASSOCIATE EDITORS MORRIS L. POVAR AND JASON MACHAN, CONSULTING EDITORS ELVA MATHIESEN, ASSISTANT EDITOR

ALLAN M. SCHRIER, FOUNDING EDITOR, 1962-1987

Published Quarterly by the Schrier Research Laboratory Department of Cognitive, Linguistic, and Psychological Sciences, Brown University Providence, Rhode Island ISSN 0023-6861

POLICY STATEMENT The Laboratory Primate Newsletter provides a central source of information about nonhuman primates and related matters to scientists who use these animals in their research and those whose work supports such research. The Newsletter (1) provides information on care and breeding of nonhuman primates for laboratory research, (2) disseminates general information and news about the world of primate research (such as announcements of meetings, research projects, sources of information, nomenclature changes), (3) helps meet the special research needs of individual investigators by publishing requests for research material or for information related to specific research problems, and (4) serves the cause of conservation of nonhuman primates by publishing information on that topic. As a rule, research articles or summaries accepted for the Newsletter have some practical implications or provide general information likely to be of interest to investigators in a variety of areas of primate research. However, special consideration will be given to articles containing data on primates not conveniently publishable elsewhere. General descriptions of current research projects on primates will also be welcome. The Newsletter appears quarterly and is intended primarily for persons doing research with nonhuman primates. Back issues may be purchased for $10.00 each. We are no longer printing paper issues, except those we will send to subscribers who have paid in advance. We will not accept future subscriptions, unless subscribers are willing to pay $100/year. (Please make checks payable to the Brown University Psychology Department.) Readers with access to electronic mail may receive a notice when a new issue is put on the Website by sending the message subscribe LPN-WARN your-own-name to [email protected]. (Send the message subscribe LPN-PDF to receive PDF files by e-mail; or the message subscribe LPN-L to receive the nongraphic contents of each issue.) Current and back issues of the Newsletter are available on the World Wide Web at . Persons who have absolutely no access to the Web, or to the electronic mailing, may ask to have paper copies sent to them. The publication lag is typically no longer than the three months between issues and can be as short as a few weeks. The deadline for inclusion of a note or article in any given issue of the Newsletter has in practice been somewhat flexible, but is technically the tenth of December, March, June, or September, depending on which issue is scheduled to appear next. Reprints will not be supplied under any circumstances, but authors may reproduce their own articles in any quantity. PREPARATION OF ARTICLES FOR THE NEWSLETTER. – Articles, notes, and announcements may be submitted by mail, e-mail, or computer disk, but a printed copy of manuscripts of any length or complexity should also be sent by regular mail. Articles in the References section should be referred to in the text by author(s) and date of publication, e.g., Smith (1960) or (Smith & Jones, 1962). Names of journals should be spelled out completely in the References section. Latin names of primates should be indicated at least once in each note and article. In general, to avoid inconsistencies within the Newsletter, the Latin names used will be those in Mammal Species of The World: A Taxonomic and Geographic Reference, 2nd Ed. D. E. Wilson & D. M. Reeder (Eds.). Washington, DC: Smithsonian Institution Press, 1993. For an introduction to and review of primate nomenclature see The Pictorial Guide to the Living Primates, by N. Rowe, Pogonias Press, 1996. All correspondence concerning the Newsletter should be addressed to: Judith E. Schrier, Department of Cognitive, Linguistic, and Psychological Sciences, Box 1853, Brown University Providence, Rhode Island 02912 [401-863-2511; FAX: 401-863-1300] e-mail address: [email protected] Current and back issues of the Newsletter are available on the World Wide Web at http://brown.edu/primate ACKNOWLEDGMENTS The Newsletter is supported by Brown University. Cover photograph of a bonobo (Pan paniscus), three year old Vic, visiting with his friend, a three year old boy in red. Taken at the Cincinnati Zoo and Botanical Gardens by Marian Brickner, June 2, 2006. Copyright © 2011 by Brown University Laboratory Primate Newsletter, 2011, 50[1]

Dead Infant Carrying in the Hanuman Langur (Semnopithecus entellus) Around Jodhpur (Rajasthan) Goutam Sharma, Bharti Swami, Chena Ram, and L. S. Rajpurohit Animal Behaviour Unit, Department of Zoology, Jai Narain Vyas University, Jodhpur Introduction studied and the most adaptable south Asian colobine.  The young of many mammalian species provide a They live in a wide range of habitats from the Himalayas variety of stimuli which influence vital parental re- and peninsular forests to semiarid lands, in villages and sponses. Bell & Harper (1977) state that primate and towns, and on cultivated land (Roonwal & Mohnot, other mammalian young “must emit the appropriate cues 1977). and possess the necessary response capabilities to ensure Data presented here are from a continuing seven-year- that care giving is released and functional.” Ethologists long study of the free-ranging langurs around Jodhpur and comparative psychologists have long recognized that (India). Jodhpur is located in Rajasthan at the eastern proper care of dependent young requires that parent- edge of the Great Indian Desert. This town is surrounded offspring interactions be regulated by reciprocally ex- by semi-desert plateau, which is inhabited by a geo- changed signals, and it is becoming increasingly clear that graphically isolated population of about 1850 langurs, both parent and young are endogenously tuned to detect comprising 32–34 one-male multi-female troops and 12– and react to each other’s signals. In neonate mammals, 14 all-male bands. The climate is dry, with maximum behavior is typified from birth by reciprocal stimulative temperatures about 48°C in May/June and minimum tem- relationships between parents and young, whereby the peratures around 0°C in December and January. Jodhpur neonate attracts the female, and the female presents a va- receives 90% of its scanty rainfall (annual average: 360 riety of primarily approach-inducing stimuli (Schneirla & mm) during the monsoon (July to September). Rosenblatt, 1961). Alley (1980) states that the distinctive markings and coloration found in young infants of many The natural open scrub vegetation is dominated by primate species function as signals which tend to “re- xerophytic plants, including Prosopis juliflora, Prosopis lease” caregiving responses. cinararia, Acacia senegal, and Euphorbia caducifolia. The langurs feed on about 190 wild and cultivated plant Jay (1962) suggests that three important elements species (for ecology, see Mohnot, 1974; Winkler, 1981; (coat color, vocalizations, and quality of movements) in and Srivastava, 1989). For religious reasons local people the infant’s appearance and behavior are essential in re- provision most of the groups with vegetables, fruits, nuts, leasing maternal behavior of the mother (or other adult and cooked or uncooked food. In some groups the provi- females) in langurs. Thus the body of a dead infant may sioning accounts for about two thirds of the total feeding continue to elicit maternal behavior (such as carrying and time. Some groups raid crops and orchards but, because grooming) from its mother and other adult females for they are considered to be sacred, these langurs are never several days after death. The carrying of dead infants has hunted. Apart from feral dogs, there are no natural preda- been reported for several primate species in the wild: Van tors in this area. The animals are easy to observe since Lawick-Goodall (1967) in the chimpanzee (Pan trog- they are not shy and spend most of the day on the ground. lodites); Schaller (1963) in the gorilla (G. gorilla gorilla); DeVore (1963) in savannah baboons (Papio cynocepha- The reproductive units are one-male multi-female lus); Kummer (1968) in hamadrayas baboons (Papio h. troops with a single adult resident male. As a rule in this hamadryas); Prakash (1962) and Alley (1980) in rhesus species, males never carry or feed infants. Each troop 2 macaques (Macaca mulatta); Rahaman & Parthasarathy occupies its own home range of about 0.5–1.5 km . With (1969) in bonnet macaques (M. radiata); Merz (1978) in few exceptions, females remain for life in their natal barbary macaques (M. sylvanus); Bowden et al. (1967), troops. Males emigrate, usually as juveniles, to all-male 2 Cleve (1969), and Kaplan (1973) in squirrel monkeys bands, whose home ranges can be as large as 20 km . (Saimiri sciureus); and Jay (1962, 1963), Mohnot (1974, According to censuses carried out in 1983–1986 (Mohnot 1977), Hrdy (1976), Rajpurohit (1987, 1992), and et al., 1987), 1990 (Rajpurohit & Sommer, 1991), 1997– Winkler, Sommer, Bornes, and Paul (pers. communica- 2001 (Rajpurohit, 1992), and 2005 (Rajpurohit et al., tions) in the Hanuman langur (Semnopithecus entellus). 2006), the number of one-male multi-female troops varied between 32 and 34. The mean troop size was 38.5 mem- Subjects and Method bers (range, 7–124 animals). The number of all-male The Hanuman langur (Dufresne, 1797) is the best bands was about 13, and averaged 11.8 members (range, 2–47 members). The mean annual population consisted

of 101.4 adult males (age > 7–8 years) and 500.5 adult  Dr. Goutam Sharma, Animal Behaviour Unit, Dept of Zool- ogy, Jai Narain Vyas University, Jodhpur–342005 (Rajasthan), females (ages > 3–4 years), yielding a mean of 17.4 re- India [e-mail: [email protected]]. productive females per troop. Male–female sex ratio at

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Location of troop Troop Troop Dates Cause of Approximate age Age of Duration around Jodhpur No. size Death of infant at death mother (days) Feb-2009 Stillbirth 0 months younger 4 Daijar B-1 127 Oct-2008 Natural 3 months younger 8 Beriganga B-3 92 Mar-2009 Stillbirth 0 months younger 7 Mandore B-6 39 Sep-2008 Natural 2 months younger 10 Mandore B-7 111 May-2010 Natural 4 months younger 9 Kaga B-11 32 Aug-2008 Natural 3 months elderly 27 Kailana B-19 13 Dec-2009 Mishandling 5 months younger 6 Bijolai B-21 48 Nov-2009 Stillbirth 0 months younger 3 Kadamkhandi B-26 47 Jan-2010 Natural 3 months elderly 17 Bhadreswar B-28 53 Jun-2010 Natural 1 month younger 3 Length of time dead infants were carried by their mothers: Range = 3–27 days (average = 9.4).

Table 1: Keeping of dead infants by mothers in Hanuman langurs, Semnopithecus entellus (Jodhpur 2008–2010). birth was 1.1 : 1, which among adults is female biased: 1 : corpse, completely decomposed, was somehow hung on a 4.1 (Rajpurohit & Sommer, 1991). All-male bands in- tree branch. For the next week, the mother was frequently vade home ranges of one-male multi-female troops in an seen sitting near the decomposed body. unpredictable pattern, sometimes resulting in rapid or Of the 10 infant deaths, 3 were newborns found dead gradual replacement of the resident male (Sommer & Raj- (considered stillbirths), 6 were natural deaths due to un- purohit, 1989). known causes, and one was due to mishandling, i.e., suf- The Hanuman langur infant stage I (“black coat”) lasts focation or choking – inexperienced mothers press infants from birth to 5–6 months; stage II (white or brown coat) hard during nursing and “kissing” and during infant trans- lasts until weaning ends at about 12–15 months, when it is fer from one female to another. almost independent of its mother (Rajpurohit & Mohnot, In Kaga (troop B-11), an old female was noted carry- 1991). ing her infant for 27 days. It was a natural death of a 3- Theoretically, the age of mother, age of infant (at month-old. The dead infant became completely dry and death), cause of death, and, to some extent type of habitat, decomposed. In another case, in Kadamkhandi (troop B- should be responsible factors affecting the duration of 26), a female was observed carrying her dead infant for keeping infants after their death. Predictions are (1) 17 days. In five cases, the ages of infants on their deaths mothers should carry a dead infant longer if it died at an were less than three months old, two were 4 and 5 months early age; (2) if death is natural or due to some unknown old respectively, and the remaining three were stillbirths. cause the mother should carry the corpse longer than in The causes of death we saw are categorized as (1) mis- cases of accidents (e.g., electrocution or fall) or “mishan- handling, (2) stillbirths, and (3) “natural” (unknown dling” (see below); and (3) old mothers should carry their causes). In this study it was noted that after the dead infants longer than young females do. All these pre- change of coat color (stage I to stage II), dead infants dictions are tested in this paper. were not carried. Whenever a dead infant was seen being carried by its mother in this study site, further observation was continued every day until the carrier finally abandoned the corpse. Ten cases were observed from August, 2008, to July, 2010 (see Table 1). Observations and Results Langurs at Jodhpur breed throughout the year: births occur year round but are not uniformly distributed. Dur- ing this study, ten cases of dead infant carrying by their mothers were observed. In one case, in Kailana (B-19), an infant was killed by mishandling. We observed that this mother carried her infant for 6 days, after which the Figure 1: Dead infant being carried by its mother.

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However, the other factors, such as the age of the mother of a troop approached these mothers and spent some time and cause of death, may also affect the duration of carry- with them. Many times they tried to take dead infants and ing. We observed the range of carrying dead infants to be groom them. We interpret these activities as “sympathy” 3–27 days (average: 9.4 days). towards the mothers. Discussion Behavior of Mother These fairly prolonged observations made over two The behavior of mothers with their dead infants was eight-month periods suggest that at least some mothers observed from the day an observer encountered a female show blind attachment to their dead infants, keeping them carrying a dead infant. Usually the dead infant’s mother in their arms for surprisingly long periods (3–6 days in the managed to walk on three limbs. At feeding time the mating and 9–29 days in non-mating season). This may mother put the infant on the ground and picked it up after at first suggest, as believed by Zuckerman (1932) for the eating. In the first 2–3 days, the mother treats the dead primates, that langurs do not recognize the phenomenon infant very carefully. She watches its eyes and face again of death, and this suggestion would seem to be supported and again. Sometimes she grooms and kisses the corpse. by the continued attachment of the mother to the dead But after decomposition and drying, mothers were seen infant for long periods. However, we observed that the being careless with dead infants. After a day or longer, other members of the troop do seem to make a distinction when the corpses started smelling, some mothers were between dead and living infants. observed defending the body against crows that tried to approach it. But other mothers did not do so. Jay (1962) in the Hanuman langur, and Prakash (1962) in the rhesus monkey (Macaca mulatta), observed In troop Kaga in August, 2008, an old female was mothers carrying dead infants. Jay (1962) suggested that observed carrying a dead infant for 27 days. It was the mothers should carry dead infants longer when they died longest period that a mother langur carried a dead infant at an early age. As an infant’s coat color changes, the during this study. She kept the infant’s body under her interest of adult females declines and they no longer seek legs at feeding time, and was very careful of outside in- out the infant to hold and groom it as often. It is her teraction. In troop Daijar-I in February, 2009, a female speculation that the natal coat color of a dead infant is carried her newborn dead baby with the placenta for four sufficient to initiate approach and grooming by adult fe- days. In January, 2010, in Kadamkhandi, an old female males. carried a dead infant for 17 days. Van Lawick-Goodall (1967) reports that a female Behavior of Other Troop Members chimpanzee (Pan troglodytes) carried her dead infant for three days. Schaller (1963) saw a gorilla (G. gorilla beringei) mother carry a dead infant (which died two days after birth) four days before leaving it. A case of a free- ranging group of rhesus macaques (Macaca mulatta) in the Jackoo Forest, Simla, has been reported by Camperio Ciani (1984), in which a one-year-old male infant died due to an adult male’s attack. The supposed mother took the dead body and carried it 400 m into the forest and sat there with it, without following the rest of the troop. Se- verely injured infants (due to infanticidal attacks) in Ha- numan langurs at Jodhpur were also observed being carried by their mothers or an allomother (Agoramoorthy & Mohnot, 1988; Rajpurohit, 1987; Sommer; 1987). Angst Figure 2: Troop members examining a dead infant. & Thommen (1977) also report other females carrying a The resident males ignored dead infants in the same newly injured infant in a semi-free-ranging colony of manner as they do live ones. But other adult females ap- Barbary macaques (M. sylvanus). Rahaman & Par- proached the body, touched it, and sometimes groomed it. thasarathy (1969, p. 157) report that “a dead baby is car- They responded this way for only a few minutes, and at ried for several days by its mother in bonnet macaques” feeding time they carelessly left it anywhere. The female (M. radiata). On the other hand, Merz (1978), in a study juveniles and older infants of the troop were also ob- of a free-ranging population of Barbary macaques, reports served smelling, touching, and watching the corpses. that all ages (juvenile and up) and sex classes will carry Sometimes juveniles picked up a dead infant, but in a few dead infants. minutes they left it on the ground. Rumbaugh (1965) reported a case in which a mother The mothers of dead infants kept some distance from squirrel monkey (Saimiri sciureus) continued to respond other troop members. In the first 2–3 days other females to her stillborn infant for more than six weeks while the

3 Laboratory Primate Newsletter, 2011, 50[1] infant remained in the cage with the mother and three New Delhi, for financial support under major project (No. other monkeys. Clewe (1969, p. 154) has suggested that F.34-460/2008 (SR) dt.2 Jan 2009). the presence of hair may be the crucial stimulus in this References species, since squirrel monkeys born without hair are dropped to the floor, while those born with it are held. Agoramoorthy, G., & Mohnot, S. M. (1988). Infanticide and juvenilicide in Hanuman langurs (Presbytis entel- Kaplan (1973) found that the response of the male lus) around Jodhpur, India. Human Evolution, 3, 279- squirrel monkey to a dead infant depends partly on the 296. age at which the infant dies. This kind of behavior has also been reported in savannah (Papio cynocephalus) and Alley, T. R. (1980). Infantile colouration as an elicitor of hamadryas (P. hamadryas hamadryas) baboons by caretaking behaviour in Old World primates. Pri- DeVore (1963) and Kummer et al. (1970), respectively. mates, 21, 416-429. A second hypothesis is that if infant death is due to some Angst, W., & Thommen, D. (1977). New data and a dis- accident (e.g., electrocution or fall), mothers would not cussion of infant killing in Old World monkeys and carry a corpse for as long as in the case of a natural death. apes. Folia Primatalogica, 27, 198-229. This would be because, in an accident, she has seen the incident and probably could make out that there is some- Bell, R. Q., & Harper, L. V. (1977). Child effect on thing wrong and nothing can be done; but with natural adults. Hillsdale. N J: Lawrence Erlbaum Associates. death the mother may not understand what is wrong with Bowden, D. P., & Ploog, D. (1967). Pregnancy and de- the infant and therefore may carry it for some time, as if livery behavior in the squirrel monkey (Saimiri sci- there were a chance for recovery. It may be, as Zucker- ureus). Folia Primatologica, 5, 1-42. man (1932) believed for the baboons, that langurs do not recognize the phenomenon of death, and this would seem Camperio Ciani, A. (1984). A case of infanticide in a to be supported by the continued attachment of mothers to free-ranging group of rhesus monkeys (Macaca mu- their dead infants for long periods. latta) in the Jackoo Forest, Simla, India. Primates, 25, 372-377. We predicted that old females should carry a dead infant (believing it to be unconscious) longer than Clewe, T. H. (1969). Observations on reproduction of younger females do. This might be because they are more squirrel monkeys in captivity. Journal of Reproduc- worried about their reproductive success, as the fertile tion and Fertility, Suppl. 6, S151-S156. period left for them is shorter than that of young females. DeVore, I. (1963). Mother-infant relations in free ranging In the present study it was observed that two old females baboons. In H. L. Rheingold (Ed.), Maternal behavior carried dead infants for the longest periods. Jay (1963), in mammals (pp. 305-335). New York: Wiley. however, reports, without mentioning the age of langur females, that dead infants are carried until they are de- Dufresne, P. (1797). Sur une nouvelle espèce de singe. composed. Other adult and juvenile females approach a Bulletin des Sciences par la Société Philomatique de dead infant less frequently than a live infant, and stay in Paris, 2[7], 49. contact with it for a shorter time (or not at all) than with Hrdy, S. B. (1976). Care and exploitation of non-human moving, vocalizing live infants. As in many primate spe- primate infants by conspecifics other than the mother. cies, langur mothers carry and protect dead infants for In J. S. Rosenblatt, R. A. Hinde, E. Shaw, & C. Beer days after their death, suggesting that a reason or factor (Eds.), Advances in the study of behavior, VI (pp. 101- other than lack of vocalization or movement is responsi- 158). New York: Academic Press. ble for this kind of maternal behavior. This factor might be natal coat color, as the coat color of a newborn infant Jay, P. C. (1962). Aspects of maternal behavior among of all species of Old World monkey is different from that langurs. Annals of the New York Academy of Sci- of an adult of the same species. But then it is not clear to ences, 102, 468-476. us why other females than the mother do not carry or Jay, P. C. (1963). The social behavior of the langur mon- groom a dead infant with its natal coat color, which otherwise they do with live infants. key. Ph.D. thesis, University of Chicago. Kaplan, J. (1972). Differences in the mother-infant rela- Acknowledgements tions of squirrel monkeys housed in social and re- The authors are grateful to Prof. S. M. Mohnot, stricted environments. Developmental Psychobiology, Chairman, Primate Research Center, Jodhpur, for con- 5, 43-52. tinuous encouragement, and to Prof. D. Mohan, Head, Kummer, H., (1968). Social organization of Hamadryas Department of Zoology, J.N.V. University, Jodhpur, for providing facilities and logistic support during this study. baboons: A field study. University of Chicago Press. Thanks are due to the University Grants Commission,

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Kummer, H., Goetz, W. & Angst, W. (1970). Cross- Roonwal, L., & Mohnot, S. M. 1977. Primates of South species modifications of social behaviour in baboons. Asia: Ecology, sociobiology and behaviour. Cam- In J. R. Napier & P. H. Napier (Eds.), Old World bridge: Harvard University Press. monkeys (pp. 351-363). New York: Academic Press. Rumbaugh, D. H. (1965). Maternal care in relation to Merz, E. (1978). Male-male interactions with dead in- infant behavior in the squirrel monkey. Psychological fants in Macaca sylvanus. Primates, 19, 749-754. Report, 16, 171-176. Mohnot, S. M. (1974). Ecology and behaviour of the Schneirla, T. C., & Rosenblatt, J. S., (1961). Animal Re- common Indian langur, Presbytis entellus. Ph.D. the- search. I. Behavioral organization and genesis of the sis, University of Jodhpur. social bond in insects and mammals. American Jour- nal of Orthopsychiatry, 31, 223-253. Mohnot, S. M., Agoramoorthy, G., Rajpurohit, L. S., & Srivastava, A. (1987). Ecobehavioural studies of Ha- Schaller, G. B. (1963). The mountain gorilla: Ecology numan langur, Presbytis entellus. Technical Report and behavior. University of Chicago Press. (1983-86) (pp. 1-89). MAB Project, Department of Sommer, V., & Rajpurohit, L. S. (1989). Male reproduc- Environment, Govt. of India, New Delhi. tive success in harem troops of Hanuman langur, Prakash, I. (1962). Group organization, sexual behaviour Presbytis entellus. International Journal of Primatol- and breeding season of certain Indian monkeys. Japa- ogy, 100, 293-317. nese Journal of Ecology, 12, 83-86. Sommer, V. (I987). Infanticide among free-ranging lan- Rahaman, H. & Parthasarathy, M. D. (1969). Studies on gurs (Presbytis entellus) at Jodhpur (Rajasthan / In- the social behaviour of bonnet monkeys. Primates, 10, dia): Recent observations and reconsideration of hy- 149-162. pothesis. Primates, 28, 163-197. Rajpurohit, L. S. (1992). Origin and composition of the Srivastava, A. (1992). The honorary uncle. BBC Wildlife, unisexual unit: An all male band in Hanuman langurs, 10, 25-32. Presbytis entellus, around Jodhpur, India. Primate Re- Srivastava, A. (1989). Feeding ecology and behaviour of port, 34, 47-52. Hanuman 1angur, Presbytis entellus. Ph.D. Thesis, Rajpurohit, L. S. (1992). Mother-infant bond and dead University of Jodhpur. infant carrying behaviour of female langurs, Presbytis Van Lawick-Goodall, J. (1967). Mother-offspring rela- entellus. Abstracts–XIVth Congress of the Interna- tionship in free-ranging chimpanzees. In: D. Morris tional Primatological Society (p. 216). August, 1992, (Ed.), Primate ethology (pp. 287-346). London: Wei- Strasbourg. denfeld and Nielson. Rajpurohit, L. S. (1987). Male social organization in Ha- Winkler, P. (1981). Zur oko-ethologe freilehender Hanu- numan langurs (Presbytis entellus). Ph.D. Thesis, man langur (Presbytis entellus entellus) Dufresen University of Jodhpur. [sic], 1797) in Jodhpur (Rajasthan), Indien. Ph.D. Rajpurohit, L. S., & Mohnot, S. M. (1991). The process of Thesis, Göttingen: George-August Universität. weaning in Hanuman langurs, Presbytis entellus. Pri- Zuckerman, S. (1932). The social life of monkeys and mates, 32, 213-218. apes. London: Kegan Paul, Trench, Trubner & Co. * * *

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Rita the Chimpanzee (Pan troglodytes ellioti): The Start of an Enrichment Program at the Doha Zoo, Qatar Hilda Tresz Phoenix Zoo  When the word “success” is mentioned in this arti- dents began manufacturing behavioral enrichment cle, readers should look for the real meaning behind it. items for the chimpanzees at Doha Zoo. During this Success in this story is not simply improving the life of time Jenny noticed that a female chimpanzee, Rita, a solitary chimpanzee somewhere in a zoo. This arti- was kept separated from the zoo’s pair, Timmy and cle shows the year-and-a-half-long, incredible team- Tina. Rita and the pair had no visual or tactile contact, work of a group of people from several different coun- and limited olfactory and acoustic contact, since their tries, who made something wonderful happen. This exhibits were far apart. program was achieved despite monetary problems, cultural and religious differences, diverse life and work styles, different levels of knowledge and training, different ages (from 8 to 60), language barriers, computer problems, and time zone differences. When people were ready to learn and work, and wanted to make a difference for the greater good, they did so. This article outlines the coordinated efforts of a group of selfless American teachers and diverse animal care professionals who started a program that made a difference, not only in the lives of the animals, but in the lives of the Doha Zoo staff and the local Qatari zoo visitors. “Bismillah ir-Rahman ir-Rahim” For an “animal person”, helping to improve an Figure 1: Jenny and Barb with Head Keeper of chimpanzees, Mohammed Tariq. Photo by Chris Wilson. animal’s life is always rewarding. In Qatar the idea is supported by Islam, which encourages people to do On March 21, 2009, Jenny contacted Dr. Jane good by their animals at all times. “People once asked Goodall, asking for instructions regarding potential Prophet Muhammad … ‘does God reward us when we improvements for Rita’s life. On March 23, Dr. Vir- treat animals well?’ Muhammad (Peace be upon Him) ginia Landau, Director of ChimpanZoo, a program of answered: ‘There’s a reward for acts of charity to the Jane Goodall Institute, directed the assignment to every beast alive.’” (Mishkat al Masabih, Book 6, me, and preparations began immediately. The essen- Chapter 6). Therefore, starting a program that would tial first step was to get support from the management improve animals’ lives would be a very desirable task. of the Doha Zoo. Jenny, already familiar with the Zoo Coupled with the wisdom of Hamad Salih al-Yazeedi, and acquainted with Hamad Salih al-Yazeedi, became the Head of Doha Zoo (clearly a man of vision who the “middle man” between me and the Zoo. thinks outside the box), it became a successful program that was praised on several occasions even by Jenny’s role was to create a report of the current Gulf News. situation, find resources to accomplish plans, involve teachers and students of the Learning Center School History and the American School of Doha in developing enrichment ideas, coordinate the manufacturing of en- Jenny Stands Wilson and Barbara Wilson (not re- richment items, conduct and record behavioral obser- lated) were teachers at the Learning Center School and vations, provide constant communication between me the American School of Doha in Qatar. Jenny and (the ChimpanZoo coordinator) and Doha Zoo man- Barb’s students were part of Jane Goodall’s Roots & agement, and document proceedings by written reports Shoots program, which teaches children all over the (accompanied with pictures and videos) to Doha Zoo world to show care and concern for animals, people, management and me. and the environment. As part of this program the stu- On Monday, April 13, 2009, Jenny learned that the  Author’s address: 455 N. Galvin Pkwy, Phoenix, AZ 85008 Doha Zoo had agreed to work with ChimpanZoo. [e-mail: [email protected]].

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Rita Short-Term Goals: To provide immediate relief. Rita’s origin was unclear. She was approximately Enrichment ideas needed to be simple, free, delivered quickly, easy to supply, safe, non-threatening, and 10 years old when the enrichment program started and had been housed alone all her life due to an unsuccess- introduced one step at a time. Due to Rita’s fairly ful introduction to Timmy and Tina, when they were empty concrete cage, the choice of enrichments that first came to mind was: all babies. Also, it was believed that she was a different subspecies from the pair. She was kept in a con- 1. Substrate to increase foraging time and for nest crete cage with metal bars, some wooden furniture, and building. 2. Browse to increase foraging time and for nest a tire, but no other objects to manipulate. building. 3. Variation of current diet presentation to increase foraging time (as in scattering and hiding chopped basic diet, and introducing novelty food items). 4. Manipulative items (toys, paper boxes, etc.) for playing and to increase foraging time. Substrate was the first choice of enrichment because it was multi-purpose. Besides helping with foraging and nest building, substrate also was free (dry leaves, donated paper and clothing, soil, etc.) or cheap (hay, straw, etc.) and helped prevent health problems caused by wet or hot concrete. However, in Qatar there were some cultural problems that prevented the use of substrates in exhibits. When visitors saw keepers scattering food in the outside cage, they demanded to be able to do the same. People also threw cigarettes inside exhibits, threatening fire within the cages. This is still an issue. Al- though the security guards were trained to watch visi- tor activities, it never became truly safe. The Zoo is Figure 2: Rita alone. Photo by Barbara Wilson working on educating the public on this issue. Rita Goals also contributed to the problem herself, by refusing to go inside when outside substrate was available. Rita The primary goal was to develop a program which felt too comfortable to leave her outside nest in the would elicit species-appropriate behaviors, using the evenings. Dry substrates such as shredded paper or limited available supplies. Following the daily activity hay were taken out of the exhibit and are now provided budget of wild chimpanzees (Figure 3), it was decided only in the night house. Outside, only sand is used. to start by immediately providing Rita with sleeping and resting opportunities, as well as by helping her to spend most of her awake time foraging and playing.

Figure 3: Average 24-hour cycle of a wild chimpanzee (per- centages of 24 hours), from L. Brent: The care and manage- Figure 4: Rita receives paper the first time in her life, April ment of captive chimpanzees (p. 18). 28, 2009. Photo by Barbara Wilson

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Browse was the next logical step. Browse is one of items included a basketball, tennis balls, logs, clothing, the most important elements of foraging. It extends plastic tubing, a mortar and pestle, a necklace, mirrors, foraging time up to several hours, provides fiber, and cleaning brushes, a toothbrush and toothpaste, plastic has practically no nutrition value. It is the best mate- dishes, and wicker baskets. rial for nest building for chimpanzees. It is also free if Long-term plans: Once the basic enrichment program cultivated and harvested on the grounds. was in place, it was time to work on long-term goals: However, there were obstacles to providing browse 1. Creating reusable/permanent fixtures that elicit as well. Green, leafy branches are difficult to come by species-appropriate behaviors. in the desert. Most of the plants available were euca- 2. Finding resources to fund these projects. lyptus and date palm species. Eucalyptus is inedible 3. Documenting enrichment. by chimpanzees, and the date palm caused some blood 4. Companionship for Rita. in the stool. Finding other sources was a challenge, 5. Educating staff to continue with enrichment. due to lack of plant knowledge and local language dif- Creating reusable/permanent fixtures: Keeping in ferences. A request for information about edible plants mind the goals of stimulating basic chimpanzee behav- specific to that region was sent all over the world, and iors (Figure 3), the features designed first were to sup- was answered by the Tel-Aviv Zoo and Haifa Univer- port resting, sleeping, foraging, and manipulating be- sity of Israel. Pictures of local trees and bushes were haviors. These were a metal sleeping basket and a taken by Jenny Wilson and sent to the Phoenix Zoo metal puzzle feeder. The basket (Figure 6) allowed and to UNESCO for identification. I also sent a list of Rita to sleep high in the “canopy”, in a stable, perma- edible plants suitable for browse (by scientific and nent nest, feeling safe and secure for the first time in common names) to the Doha Zoo veterinarian, who is her life – just as she would have felt in the wild. The successfully giving the chimpanzees acacia now. puzzle feeder was a locked, simple mesh cage which Variable presentation of the current diet was a high was easy to clean and refill without taking too much of priority, since it is an important part of foraging. Ini- the keepers’ time. Originally it was placed in a fairly tially, only those methods were chosen that were fast, high area, but it turned out to be hard to reach for the free, and could be immediately implemented. Feed- keepers to fill. It has not yet been moved and is cur- ings were increased from once to twice per day. Food rently not being used. was chopped into very small pieces (but not diced so Finding resources. What can be done, and what small that Rita would not bother gathering them) and should be done, as well as issues of time, money and scattered on the floor, and hidden in substrates or on manpower, were resolved by organizing a support sys- furniture. However, scattering food could not be con- tem. All enrichment items were made by Qatari school tinued, due to both keeper workload and problems with children and their teachers and then distributed during visitors seeing food in the cage. the weekends. Three groups belonged to Jane Goodall’s Roots & Shoots program and, as such, spent most of the weekends observing and documenting that enrichment at the Doha Zoo. Besides their time they also provided almost all of the financial support. Documenting enrichment. Experience shows that keeping up with documentation is one of the hardest tasks in any program. When it comes to inventing and implementing new ideas, creativity almost always out- paces resources, such as time, money, and staffing. The collection of data by students, even as young as 8 to 12 years, served several very important purposes. When the children could observe their enrichment items being used with their own eyes, they could also prove the usefulness of their enrichments by docu- Figure 5: Doha Zoo staff hiding food in substrate on exhibit. menting the chimpanzees’ behavior with them and Photo by Barbara Wilson. then evaluating the items during classes – certainly a successful teaching/learning process. Having the stu- Manipulative items. Rita received many non-food- dents and teachers helping out also freed up some time related enrichments that she could play with. Items for the Doha Zoo staff; however, sometimes the over- included paper products such as cardboard tubes and whelming amount of incoming enrichment items cre- boxes, wrapping paper, books, ribbons, etc. Other

8 Laboratory Primate Newsletter, 2011, 50[1] ated extra work for them. In gratitude the kids make thank-you cards and gift boxes for the staff. Companionship for Rita. Naturally, Rita’s new enrichment program also affected the other two chimpanzees’ lives, as Timmy and Tina received items similar to hers. It is well known that of all enrichment categories, social enrichment is the highest priority for any species that do not lead solitary lives. The integration of the three chimpanzees was imperative. With the help of the Institute of Vertebrate Biology, Academy of Sci- ences of the Czech Republic, it was ascertained that all three chimpanzees were the same subspecies, matched on the matrilineal side. The three chimpanzees were successfully introduced to each other in June of 2010. The details of the introduction will be described in a separate article. Educating Staff. New programs and new ideas cannot be successfully implemented without the staff fully understanding the reasons behind them. The ideas need to be plausible, and staff need to understand the final outcomes as well as all the details that will lead to accomplishing them. The Doha Zoo manage- Figure 6: Rita in new basket nest. Photo by Barbara Wil- ment worked continuously with its staff and provided son. help whenever possible to make the new program happen. Everybody was on board! In June, 2010, because Acknowledgements of the increasing enrichment programs, and to ensure Special thanks to all the people who participated in continuing education of staff, The Doha Zoo organized this project: Hamad Salih al-Yazeedi, Mohammed its first five-day enrichment workshop. Beyond a Hussein Hassan, Moza Ahmed al-Qahtani, Abubaker doubt this opened people’s eyes to the endless possi- Hamuda, DVM, Selma al-Shaik, Mohammed Abdul- bilities which can improve animal welfare. raheem, Mohammed Nurnobi Chowdhory, Mohammed Discussion Tariq, Jenny Stands Wilson, Chris Wilson, Barbara Wilson, Jody Kruger, Tawney Kruger, Andra Vizante, “He is not a perfect believer, who goes to bed full Joyce Liberto, Peter Vallo, PhD, Klara J. Petrzelkova, and knows that his neighbor is hungry” (Mishkat al PhD, Mwanahamissi Issa Mapua, BSc, Josef Masabih, Book 2, Chapter 424) is truly a phrase that Bryja, PhD, Benno Boer, PhD, Itai Roffman, Ori should guide us all regardless of our beliefs. No one Pomerantz, Julie Swenson, DVM, the Learning Center should walk by any unwanted situation and not do School of Qatar Foundation, the American School of something about it, whether the motivation is from Doha, Qatar Academy School, and the American religious principles or one’s own conscience – or any Women’s Association of Doha. other reason. And no one needs to feel alone in doing so, either. The story of Rita illustrates this. She went The Arabic phrase “Bismillah ir-Rahman ir- from being a lonely chimpanzee to a well-adjusted Rahim” is often said when one is embarking on any animal living in a small but functioning social group, significant endeavor. It is a beautifully poetic expres- receiving enrichment daily and exhibiting species- sion which offers both insight and inspiration. It is appropriate behaviors. All thanks are due to a group of almost impossible to capture either the true depth of people and their continuous efforts to do better. In meaning or the inspirational message of this beauti- return Rita touched their souls, and by doing so en- ful phrase by simply translating it. One poetic trans- couraged them to do more, not just for her but for all lation is: “Every moment of this life is filled with your animals. As a result, an enrichment program that first eternal radiance, my Beloved, You are the Beneficent focused on one individual chimpanzee and then on two One who endlessly showers all of creation with nour- others, has spread out to more species that needed im- ishment and blessings, and the One who generously mediate help, and from there has developed into a zoo- rewards those who live in harmony with Your wide program. What more can one want? Is this not Divine Will.” For further information see: the real meaning of success? .

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Separating Cage-Mates Temporarily – A LAREF Discussion On November 15, Viktor Reinhardt posted the following to the LAREF when a partner isn’t available.” (Laboratory Animal Refinement & Enrichment Forum) Erik Moreau , an animal e-mail discussion list: health technician from a contract research organization in “Research protocols sometimes require that compati- Montreal, wrote: ble macaque pairs be physically separated for a limited “The animals are separated with visual, olfactory, and time period (e.g., controlled food-intake studies; sample limited physical contact through a wire-mesh separator.” collection from chair-restrained subjects). Later that same day, Viktor posted another query: “Obviously – and as documented in the literature – “Are any of you aware of published studies assessing partner separation is a stressful event that not only has stress parameters of macaques who maintained visual animal welfare implications but can also skew subse- contact during physical, research-related separation versus quently collected research data. those who were separated by moving one animal out of “If pair-housed macaques in your care have to be the room?” separated, (a) what do you do to minimize the stress for Marcie Donnelly re- the animals; or, if you don’t have the authority, (b) what sponded: would you do to minimize the stress for the animals?” “I am not aware of any published studies, but I would Thomas Ferrell guess there are some out there. responded: “We do on occasion take a partner out for a pharma- “We use either a single-wire divider panel or a solid cokinetic study – but they would only be removed from Plexiglass panel, depending on the situation. In either the room for about nine hours (the day pretty much), then case, separation is for the shortest time possible.” returned and fed. Many times they remain in visual con- Melissa Truelove , of the Be- tact overnight to allow the monkeys to eat. If they finish havioral Management Unit at Yerkes NRPC, wrote: eating everything before we go home they are returned to “Allow maximum visual contact (e.g., lexan [trans- pair housing for overnight. parent] solid panel if monkeys can tolerate it) during “In the past we have had to separate monkeys for fe- separation period or maximum limited physical contact ces / urine collection, as well as food consumption, and (e.g., perforated panels) with their partner(s). I’ve worked we have kept the partners on visual access via mesh. with several pairs who have remained separated for pro- They do well and are able to be re-paired. This would be jects for more than two months with a solid lexan panel in for one week generally – we did have a pair of girls and place and successfully returned to pair housing following one would not eat well while separated from her partner – completion of the project. From a behavioral manage- makes you sad for sure. It also tells you there is some ment perspective, it made the reintroductions easier as the stress related to the separation. They have visual, tactile animals maintained visual (and thus social) contact for the (but the screens are small), and olfactory contact, but they duration of the required separation. The same can be said can’t be next to one another and groom, or eat next to for separation using perforated panels. These types of each other. I think that can be really hard for them.” separation should be less disruptive than total separation from a partner, thus should minimize stress. Also a pri- * * *

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Meeting Announcements The Third East Mediterranean ICLAS Symposium, hold its 2011 Forum in Denver, Colorado, June 15–18. organized by the Laboratory Animal Science Association See . for Laboratory Animal Science (ICLAS), will be held in In association with BioMed Central, the Society of the city of Istanbul, Turkey, June 13–15, 2011. The sym- Chinese Bioscientists in America’s 13th International posium is open to everyone interested in Laboratory Ani- Symposium ‘Bioscience for the 21st century: Emerg- mal Science and experimental studies. Many topics will ing Frontiers and Evolving Concepts’, takes place in be under discussion, including ethical evaluation, Guangzhou, China, July 25–-29, 2011. Visit the experimental design, new technologies in laboratory conference Website, < >, animal science, animal models, methods for reduction, www.scbameeting2011.org etc. Siyami Karahan, President of (LASA)–Turkey, for further information. Then, register at ; welcomes you to submit abstracts for oral or poster and submit your abstract at . . The American College of Veterinary Internal The 13th Congress of the European Society for Medicine (ACVIM), the mission of which is to enhance Evolutionary Biology will be held in Tübingen, Ger- animal and human health by advancing veterinary internal many, from August 20–25, 2011. See medicine through training, education, and discovery, will . * * * Information Requested or Available Great Apes in Japan chairs) to enter content directly. Be patient; it should be worth it! The Great Ape Information Network has created an English homepage and database on great apes living in Interesting Websites Japan: . The Network writes, “Though some parts are still only in  Animal Welfare Institute’s AWI Quarterly: New ASP Website  Kyoto University’s Primate Research Institute’s Section of Language and Intelligence Links: Website, at , with a complete redesign by a professional designer. There is still content to be  Medical Coding’s Medical Science Publications: incorporated into the new Website; it is not fully complete Website, and a few may redirect to a broken link, as those  National Association for Biomedical Research’s animal pages have not been entered yet. The programming is law Website: < > complex because all content will now be in a database NABRAnimalLaw.org (instead of as static html), and an interface has been cre-  The Animal Aging and Longevity Database: ated that will allow specific people (such as committee * * *

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Resources Available Special OLAW Online Seminar  Schedules - FR, FI, VR, VI, Progressive Ratio. “AC and OLAW Perspective on Nonhuman Primate The CANTAB Catalog may be downloaded at: Enrichment and Social Housing” was recorded by the . Animal Welfare (OLAW); U.S. Department of Agriculture (USDA), Animal and Plant Health If you have questions, you can contact Vern E. David- Inspection Service (APHIS), Animal Care (AC); and son, Neuroscience Product Manager, Lafayette Instrument USDA, National Agricultural Library (NAL), Animal Co. [765-423-1505, Ext. 206; Fax: 765-423-4111; e-mail: Welfare Information Center (AWIC) on June 11, 2010. [email protected]]. The seminar can be viewed as Power Point at , or as a Marian Brickner, some of whose bonobo photographs PDF file at . has produced a beautiful 2011 calendar, which is Speakers at the Seminar were Dr. Robert Willems, available on a CD for $7, including U.S. postage. See Assistant Regional Director, Eastern Region, USDA, , APHIS, AC; Dr. Axel Wolff, OLAW, Director, Division or contact her (766 Harvard Ave, St. Louis, MO of Compliance Oversight; and Ms. Kristina Adams, 63130 [314-680-4333; e-mail: insect1 @swbell.net]). Technical Information Specialist, USDA, NAL, AWIC. Hominoid Carrying Archive Online Moderators were Dr. Jerry Collins, OLAW, Division of Policy and Education and Yale University; and Ms. Dr. Bill Sellers, of the University of Manchester, Susan Silk, OLAW, Director, Division of Policy and announces the availability of the Hominoid Carrying Education. Archive online. This is a large collection of video data collected as part of a Natural Environment Research The subject of the presentation is social housing of Council project into the carrying behavior of great apes. nonhuman primates in a research setting. Social housing The video is in standard digital format with an Audio is a part of the enrichment program for nonhuman pri- Video Interleave wrapper that should be readable by mates required by the Animal Welfare Act regulations. almost any video software. Basic joint center motion Dr. Willems presented the regulatory requirements for capture was performed by hand for almost all the clips social housing of nonhuman primates and covered the presented and this data is available too. Hopefully you allowable exceptions to that requirement. will find some of this information useful for teaching or research and you can access the library through the Questions may be submitted to OLAW [e-mail: Animal Simulation Laboratory Website at [email protected]]. . CANTAB Cognitive Testing System For more information, contact Dr. Sellers at the The IntelliStation T is the latest development in the Fac. of Life Sciences, Univ. of Manchester, 3.614 CANTAB Cognitive Testing system for nonhuman pri- Stopford Bldg, Oxford Rd, Manchester, M13 9PT, mates. It retains all the test-specific criteria, stimulus U.K. [e-mail: [email protected]]. presentation, and animal response/reward hardware of all past systems. The application portfolio comprises a bat- Procedures with Care tery of tests performed via a touch screen. Test protocols Paul Flecknell, of the Comparative Biology Centre at are flexible and can be configured by the user. Multiple the Medical School in Newcastle, U.K., announces the tests may be linked in the same subject session. launching of a new Website, the development of Monkey CANTAB is comprised of the following: which was co-funded by the IAT and NC3Rs: . He writes, “We will be adding more material to the site over the next month or  Training Program, so. At present it covers a series of injection techniques  Intra/Extra-Dimensional Set-Shift and Visual with rat and mouse, and on each ‘procedure’ page there is Discrimination (ID/ED), a ‘trainer’s pack’ that lets you download the video and  Delayed Match / Non-Match to Sample, still images for use in your own training activities.”  Spatial Working Memory,  Five-Choice Serial Reaction-Time Task, We look forward to the addition of nonhuman pri-  Paired Associates Learning, and mates to the animals covered on this site.

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Lincoln Park Zoo’s Blood Type Database for Apes tered into a database coordinated at the the Zoo’s Lester E. Fisher Center for the Study and Conservation of Apes At present, no standard blood type data has been determined for the great ape (gorillas, chimpanzees, bono- . Eldon Biologicals donated the bloodtyping cards that bos and orangutans) population in zoos. The knowledge are used and validation of the cards is being performed at of blood types would provide better acute veterinary the University of Chicago, since the cards were designed medical care, and reduce transfusion reactions by know- for human blood types. The project has grown signifi- ing compatibility of donor and patient blood. cantly, to include not only all accredited zoos that house great apes in North America, but also populations in In March of 2006 Veterinarian Dr. Kathryn Gamble European zoos (EEP), PASA (Pan African Sanctuary Al- and Master Keeper Jill Moyse started the project “Cata- liance) sanctuaries, and the Nyaru Menteng Orangutan loging blood types for SSP populations of great apes”, Rehabilitation Center. As of 2009, they had received 539 which aims to gather and test blood samples from zoo completed blood typing cards. They now have typed apes as they undergo their routine physicals. All four blood from about 700 animals around the world. – from great ape species are being tested and the results are en- the Lincoln Park Zoo Webpage, and a December 5, 2010, article in the Chicago Sun-Times * * * Resources Wanted: Videos of the Birthing Process “Lisa Pfeifer, currently a graduate student in the De- ing the birthing process. She is trying to assemble a col- partment of Biology at the University of Maryland, Col- lection with as many different species as possible, includ- lege Park, is working on developing a course on the evo- ing both wild and captive animals. Please contact her [e- lution of human birth and would like to have examples of mail: [email protected]] if you have one or more vid- how nonhuman primates behave, vocalize, and move dur- eos that you are willing to share.”

* * * ASLAP Veterinary Student Award Program The American Society of Laboratory Animal Practi- why the student should be recognized. Please note that tioners (ASLAP) Veterinary Student Liaison Committee students who wish to nominate themselves or another (VSLC) is seeking nominations of veterinary students for student must be members of the national ASLAP organi- the Society’s annual Veterinary Student Award Program zation. Nominations must be received by January 14, (VSAP). The VSLC, with approval of the Board of 2011, and must include contact information (including e- Directors, has recently expanded the Veterinary Student mail) for the nominee. Award Program to allow for one award to be given at Nominees will be asked to submit a current CV and an each veterinary school. Last year 25 awards were given. essay of up to 500 words describing their participation in The VSAP is intended to increase awareness of the activities related to laboratory animal medicine and how practice of laboratory animal medicine by recognizing these activities have influenced their interests and career students who have demonstrated significant interest and goals. Information will be evaluated by the Veterinary potential in the field. Awards (a certificate, one year’s Student Liaison Committee. membership in ASLAP, and a cash sum of $300) will be Please send nominations to Judy Daviau [e-mail: ju- presented at each school during their awards program or [email protected]]. another suitable public event involving a large proportion of the student body. Please support and encourage a veterinary student you know who is interested in laboratory animal medicine by Nominations are welcomed and encouraged from any nominating them for this award. current national ASLAP member and should be accompanied by a brief statement from the member that explains * * *

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Research and Educational Opportunities Veterinary Residency, New York nardini, Via Caldera 21, 20153, Milano, Italy [02- 45076787; fax: 02-45070212; e-mail: secretary@ The Institute of Comparative Medicine at Columbia fondazioneguidobernardini.org]. University has a postdoctoral research scientist position available for a highly motivated veterinarian with a back- Wildlife Studies and Primatology – Japan ground in veterinary practice and comparative medicine The Primate Research Institute and the Wildlife Re- (Requisition # 0001696). The residency in Comparative search Center, both affiliated with Kyoto University, have Medicine focuses on phenomena basic to disease in all launched a new graduate program, the Center for Interna- species, including humans, and provides a challenging tional Collaboration and Advanced Studies in Primatol- intellectual opportunity to work with medical, biomedical ogy, aimed at facilitating international collaboration and and veterinary specialists. The residency prepares the advanced studies in conducting multidisciplinary studies candidate for board certification by the American College of wildlife in either field or captive settings. The details of Laboratory Animal Medicine (ACLAM) and a career are available at www.pri.kyoto- in biomedical research. See . edu/dept/icm/rtp.html> for details. There are two options: Education and Training in Field Primatology 1) Residency – Main Track: This 3-year program rotates The American Society of Primatologists (ASP) will through medicine, surgery, pathology, and research, with offer two scholarships annually to outstanding under- substantial didactic and experiential components. graduate and graduate students for research and career 2) Residency – Two-Year Option: Like 1), without the training in a field course at La Suerte Biological Research research project if the applicant has already satisfied the Station, Costa Rica, or Ometepe Biological Research Sta- ACLAM requirement for research training and manu- tion, Nicaragua, funded through an educational grant from script publication. the Maderas Rainforest Conservancy (MRC). The goals Columbia University offers a competitive package, of the MRC are to advance research, education and con- including a family health program, and four weeks of servation of primates and tropical forests. Interested stu- vacation. Interested individuals should apply at dents from anywhere in the world are encouraged to apply. . mately one-month course, including room and board (3 If you have any questions, please contact Rivka meals/day), instruction, access to all facilities at the field Shoulson, DVM, MPH, Inst. of Comp. Med., Columbia site, and in-country transportation to and from the field Univ. Med. Ctr, 650 W. 168th St, BB 1810, New York, site. The scholarship does not include airfare to Costa NY 10032 [[email protected]]. Rica or Nicaragua, books, supplies, field equipment, medical insurance, or hotel/meals the first and last night Laboratory Animal Science Management Courses in San Jose (Costa Rica) or Managua (Nicaragua). Field The Guido Bernardini Foundation (FGB) is a not-for- courses are offered during December–January and from profit organization established to promote biomedical May through August. research by focusing on providing training and continuous Students awarded scholarships will be selected by the professional development for laboratory animal science ASP Awards Committee based on the strength of the stu- professionals. The FGB is pleased to announce the up- dent’s academic record, responses provided in the appli- coming Laboratory Animal Science Management Courses cation materials, and a letter of recommendation. to be held in Milan, Italy, in 2011:  TC-1: Cleansing and Decontamination: Best Practices Additional information and application instruc- www.asp.org/ in Washing, Disinfection and Sterilization in the tions and forms can be found at: < grants/scholarship/index.cfm Laboratory Animal Facility, January 25–27. >. Online submission will begin January 1, 2011. The student must submit  TC-3: Organization and Procedures in the Modern his/her completed application materials to the ASP Laboratory Animal Facility, May 16–20. Awards Committee by March 1, 2011.  TC-5: Biocontainment in the Laboratory Animal Fa- cility, November 8–9. For questions concerning the scholarship application, contact Peter Judge [e-mail: [email protected]]. For For complete information, see ; or contact Laura and field site facilities, contact Paul A. Garber [e-mail: p- De Francesco, General Secretary, Fondazione Guido Ber- [email protected]].

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Husbandry for Zoo and Aquarium Animals – Mexico and visits around the Zoo, translation if needed (English – Spanish – English), Proceedings, a Certificate of Atten- The Guadalajara Zoo and The Mexican Institute for dance, transportation (Hotel – Zoo – Hotel), coffee Wildlife and Companion Animals invite you to participate breaks, and closing lunch. in the course: “Behavioral Husbandry (Enrichment and Training) for Zoo and Aquarium Animals (Terrestrial and For information about the city, transportation, and Marine Mammals, Birds, Reptiles, Fishes)”, which will be attractions, please visit: . For more information 2011. This course is designed for zookeepers, aquarists, about and registration for this course, contact the Educa- trainers, curators, veterinarians, related career students, tional Dept, Guadalajara Zoo, Paseo del Zoológico #600, and anyone interested in the topics. A. P. 1-1494 C. P. 44390, Guadalajara, Jalisco, México The registration fee is US$150 before February 17, [Tel. +52 (33) 3674 4488 / 01 800 000 8000; Fax +52 US$200 before April 17, and US$250 after April 17. (33) 3674 3848; e-mail: mmartinez@zooguadalajara Daily rate is US$65. The fee includes: lectures, practices .com.mx and [email protected]]. * * * News Briefs Devra G. Kleiman: Conservation Biologist adopted as the most effective way to manage the genetics of rare species. It has been crucial to the suc- Devra G. Kleiman, 67, a biologist whose ground- cessful reintroduction to the wild of species including the breaking research on giant pandas and South American black-footed ferret and the California condor. – by Emma monkeys showed how zoos can play a critical role in pre- Brown, Washington Post Staff Writer, May 4, 2010 serving endangered species, died April 29 at George Washington University Hospital. She had cancer. In a Will Aging Research Chimpanzees Be Relocated? career spanning more than 40 years, much of it at the Na- tional Zoo, Dr. Kleiman helped create and define the new “Most of the chimpanzees at the Alamogordo Pri- field of conservation biology. mate Facility are well into their twenties and have not been research subjects for more than a decade. After a She was perhaps best known for spearheading an un- ten-year hiatus, the chimpanzees of the Alamogordo precedented international effort to save golden lion tama- Primate Facility in New Mexico are being called back to rins – small, reddish-orange monkeys that live in Brazil’s duty. The 186 chimps, already grizzled veterans of Atlantic coastal forests – from extinction. In the early medical research, will be pulled from an unofficial 1970s, Dr. Kleiman responded to an alarm sounded by retirement and sent back into the lab by the end of 2011, Brazilian biologist Adelmar Coimbra Filho. Golden lion the National Institutes of Health (NIH) announced in tamarins were in trouble: research showed there were only August. But the decision has brought to a head a sim- several hundred of the animals remaining in the wild and mering debate about the use of chimpanzees for medical fewer than 75 in captivity. Kleiman and Coimbra helped research in the United States – a practice banned by the persuade officials at more than a dozen zoos not to sell European Union this September. The chimps would re- their golden lion tamarins for profit. Instead, the zoos join a dwindling cadre of research primates. In 1995, the would lend the animals to one another for breeding. NIH established a moratorium on chimpanzee breeding Eventually they gave up title to the tamarins altogether, in federally supported laboratories, and scientists have ceding ownership to the Brazilian government. Dr. developed alternative ways to study the basic biology of Kleiman played monkey matchmaker, using genetic data diseases. But the roughly 700 chimps remaining still to determine which animals should mate to create strong have a key role in vaccine testing for viruses such as offspring. hepatitis C and HIV, which don’t infect other laboratory Those offspring were reintroduced to Brazil, where animals.” – by H. Ledford, from Nature, October, 2010, Kleiman and Coimbra helped preserve and restore wide 467, 507-508, golden lion tamarins live in the wild. Another 500 live in 145 zoos around the world. The species’ status has been NY Must Release Records on Monkey Research changed from critically endangered to endangered, and a A judge in Albany, New York, says New York must Brazilian organization that Kleiman helped found is coor- release records on substance abuse experiments on mon- dinating efforts to ensure the species’ long-term survival. keys and other animals. The state’s Office of Mental The cooperative model Dr. Kleiman pioneered with Health tried to block the Freedom of Information Act re- the golden lion tamarin project has since been widely quest from the Physicians Committee for Responsible

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Medicine (PCRM), saying research scientists may be tar- said zoo veterinarian Dr. Graham Crawford. Unlike the geted by animal-rights terrorists. In a ruling PCRM re- other gorillas, Zura will eat cups, purses, and even cell ceived this week, state Supreme Court Justice Richard phones dropped within her reach. Platkin rejected the state’s argument. Many of the ex- “She’s had some GI issues,” said zoo primate curator periments conditioned rhesus monkeys to have drug and Corinne MacDonald, “and we’re wondering whether or alcohol addictions, then tested them to see if medications not it is because of that, or if there something else going broke the addictions. – PCRM press release, November on.” 12, 2010 As with any other patient, doctors needed to get a AVMA Revises Veterinarian’s Oath closer look, and so this first-of-its-kind here procedure The American Veterinary Medical Association called a capsule endoscopy, in which a tiny video camera (AVMA) has revised the Veterinarian’s Oath — which all is actually inserted into Zura’s intestines. “We think that graduates of U.S. veterinary schools take — to stress the probably she has Crohn’s disease, based on a lot of sero- importance of animal welfare. The revised oath, ap- logical markers, blood tests that we’ve taken on her,” said proved by the AVMA Executive Board at its meeting this gastroenterologist Dr. David Shields. month, is as follows: “Being admitted to the profession of Gorillas carry the gene for Crohn’s, a sometimes fatal veterinary medicine, I solemnly swear to use my scientific autoimmune disease. Powerful drugs can treat it. “All knowledge and skills for the benefit of society through the these drugs have risks,” said Shields. “Unless we’re sure protection of animal health and welfare, the prevention that this is the case with her, we’d like not to treat her.” and relief of animal suffering, the conservation of animal resources, the promotion of public health, and the ad- Results from the implanted camera should be avail- vancement of medical knowledge.” able in a few days. Zoo veterinarians will then decide what to do. – NECN/KTVU, December 6, 2010 “The Veterinarian’s Oath reflects every veterinarian’s aspirations for themselves and the veterinary profession,” Census: Mountain Gorilla Population Grows says Dr. Bruce Nixon, Chair-Elect of the Animal Welfare The population of mountain gorillas in their main Committee. “It’s a promise that each veterinarian makes at graduation, so these words have tremendous meaning. Central African habitat has increased by a quarter in The Animal Welfare Committee recommended these seven years, regional authorities say. Most of the world’s mountain gorillas are found in the Virunga massif, which changes to emphasize that veterinarians have responsibili- ties not only to animal health but also to animal welfare.” includes three contiguous national parks in Rwanda, the Democratic Republic of Congo (DRC) and Uganda. The “These changes make it clear that the scope of veteri- population of the iconic but endangered animal in that narians’ efforts toward improving animal welfare include area increased from 380 individuals in 2003 to 480, ac- not only treatment, but also prevention of suffering and cording to a census carried out earlier this year and promotion of good welfare, which is consistent with to- funded by a number of local and foreign wildlife organi- day’s approach to veterinary practice,” adds Dr. Gail Go- zations. lab, Director of the AVMA’s Animal Welfare Division. “The increase in mountain gorilla numbers is a testa- For more information, see . – ment that we in the Virunga massif are all reaping from AVMA Press Release, December 2, 2010, Schaumburg, the conservation efforts sowed on a daily basis,” Rica Illinois Rwigamba, of the Rwanda Development Board said. Gorilla Tested for Possible Human Disease The only place outside of the Virunga massif where mountain gorillas are found is Uganda’s Bwindi Impene- A female gorilla at the San Francisco Zoo is recover- trable National Park. Along with 302 individuals being after a unique medical procedure. This gorilla has lieved to dwell in Bwindi and four orphans living in a undergone a special kind of surgery, and a local doctor is sanctuary in DRC, the census put the known world popu- helping to diagnose what appears to be a human disease. lation of mountain gorillas at 786. At the gorilla enclosure, dominant silverback Oscar Mountain gorillas, who have fallen prey to conflict Jonesy watched intently, as technicians anesthetized his and poaching over the years, were brought to the world’s sister, 29-year-old Zura, and took her to the zoo hospital. attention by the late Dian Fossey and are one of the re- “She has had chronic medical problems with her gas- gion’s main tourist attractions. – AFP©, a news agency, trointestinal tract, mainly diarrhea, constipation, bloat,” December 7, 2010 * * *

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President Obama Honors Nation’s Top Scientists and Innovators On October 15, President Obama named ten eminent mnemonic functions and localize their critical neural researchers as recipients of the National Medal of Sci- substrates; ence, and three individuals and one team as recipients of  applying anatomical tracing techniques, to reveal how the National Medal of Technology and Innovation, the the different substrates belonging to a functional fam- highest honors bestowed by the United States government ily are organized as components of a neural system or on scientists, engineers, and inventors. circuit; Mortimer Mishkin, Chief of the Section on Cognitive  recording electrophysiological activity within the Neuroscience in the Laboratory of Neuropsychology, Na- identified substrates, to determine the nature of the in- tional Institute of Mental Health, is one of the Medal of formation those neurons receive and transmit before, Science recipients. The Section he leads uses a multidis- during, and after learning; and ciplinary approach to investigate the neurobiological  injecting pharmacological agents into those same sub- mechanisms underlying learning and memory in primates. strates, to relate the learning-dependent changes in be- In monkeys, the approach involves: havior and neuronal activity to the underlying cellular  utilizing metabolic mapping techniques, including and synaptic mechanisms. both autoradiography and neuroimaging, to delineate The learning and memory mechanisms uncovered in the cerebral territory belonging to a particular func- the research on monkeys serves as the basis for a search tional neural system; for homologous mechanisms in brain-damaged patients  studying the effects of selective lesions within that examined both neuropsychologically and with quantita- territory on the performance of specially designed tive magnetic resonance techniques. – from a White learning and memory tasks in various sensory modali- House press release ties, in the attempt to separate and identify different * * * Announcements from Publications: The Journal of Evolutionary Biology Research The Journal of Evolutionary Biology Research (JEBR) You are invited to submit your manuscript(s) to is a multidisciplinary, peer-reviewed, open access journal, for publication. JEBR at- published monthly by Academic Journals, tempts to inform authors of the decision on their manu- . JEBR is dedi- script(s) within four weeks of submission. Following cated to increasing the depth of evolutionary biology re- acceptance, a paper will normally be published in the next search across disciplines, with the ultimate aim of im- issue. Instructions for authors are available at proving evolutionary research. . JEBR welcomes the submission of manuscripts that htm meet the general criteria of significance and scientific JEBR is fully committed to the Open Access Initiative excellence in this subject area, and will publish: and provides free access to all articles as soon as they are  original articles in basic and applied research, published.  case studies, and  critical reviews, surveys, opinions, commentaries and essays. * * *

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Recent Books and Articles (Addresses are those of first authors unless otherwise indicated) Books chimpanzees, by W. C. McGrew. Part III. Social Minds: Ecological Perspectives. Chimpanzee minds in nature, by  Ape House. S. Gruen. New York: Spiegel & Grau, 2010. J. C. Mitani, S. J. Amsler, & M. E. Sobolewski; Vocal 320 pp. [Price: Hard-cover: $26] communication in chimpanzees, by K. Slocombe & K. This novel was inspired by the author’s visits to the Zuberbühler; The function and cognitive underpinnings of Great Ape Trust, in Des Moines, Iowa. It is available as an post-conflict affiliation in wild chimpanzees, by R. M. unabridged audio compact disc, an unabridged audio-book Wittig; and The role of intelligence in group hunting: Are download, an E-Book, and a large-print trade paperback, as chimpanzees different from other social predators? by I. C. well as a hard-cover. Gilby & R. C. Connor. Part IV. Social Minds: Empirical  Biologie Moleculaire et Phylogenese des Lemuriens Perspectives. Chimpanzee social cognition, by M. (Madagascar): Les Lemuriens, Primates de Madagascar. Tomasello & J. Call; Intentional communication and com- D. Montagnon. Sarrebruck, Germany: Editions Universi- prehension of the partner’s role in experimental coopera- taires Europeennes, 2010. tive tasks, by S. Hirata, N. Morimura, & K. Fuwa; Collabo-  The Encyclopedia of Applied Animal Behaviour and Wel- ration and helping in chimpanzees, by A. P. Melis, F. fare. D. S. Mills, J. N. Marchant-Forde, P. D. McGreevy, Warneken, & B. Hare; Inequity and prosocial behavior in D. B. Morton, & C. J. Nicol (Eds.). Wallingford, U.K.: chimpanzees, by S. F. Brosnan; and The need for a bottom- CABI, 2010. up approach to chimpanzee cognition, by F. B. M. de Waal. Part V. Ethics, Care, and Conservation. How cogni-  The Infanticide Controversy: Primatology and the Art of tive studies help shape our obligation for the ethical care of Field Science. A. Rees. University of Chicago Press, 2009. chimpanzees, by S. R. Ross; Positive reinforcement train- 288 pp. [Price: $40] ing, social learning, and chimpanzee welfare, by J. E.  The Mind of the Chimpanzee: Ecological and Experi- Perlman, V. Horner, M. A. Bloomsmith, S. P. Lambeth, & mental Perspectives. E. Lonsdorf, S. R. Ross, & T. Matsu- S. J. Shapiro; Chimpanzee orphans: Sanctuaries, reintro- zawa (Eds.). University of Chicago Press, 2010. [Price: duction, and cognition, by B. B. Beck; Human-chimpanzee Cloth: $125; Paper: $49; E-book: $7 to $49] competition and conflict in Africa: A case study of coexis- Contents: Foreword, by Jane Goodall; The chimpanzee tence in Bossou, Republic of Guinea, by K. J. Hockings; mind: Bridging fieldwork and laboratory work, by T. Ma- and Chimpanzee mind, behavior, and conservation, by E. tsuzawa. Part I. Cognitive Mechanisms. Early social cog- V. Lonsdorf. Afterword: Meanings of chimpanzee mind, nition in chimpanzees, by M. Myowa-Yamakoshi; Using by R. Wrangham. Appendix: Major chimpanzee research an object manipulation task as a scale for comparing cogni- sites. tive development in chimpanzees and humans, by M. Ha-  Multisensory Object Perception in the Primate Brain. M. yashi; Do the chimpanzee eyes have it? by M. Tomonaga; J. Naumer & J. Kaiser (Eds.). New York: Springer, 2010. Understanding the expression and classification of chimpanzee facial expressions, by L. A. Parr; Behavioral and  Neurobiology of Grooming Behavior. A. V. Kalueff, J. brain asymmetries in chimpanzees, by W. D. Hopkins, J. L. LaPorte, & C. L. Bergner (Eds.). Cambridge, U.K.: Taglialatela, D. A. Leavens, J. I. Russell, & S. J. Shapiro; Cambridge University Press, 2010. and Trapping the minds of apes: Causal knowledge and inferential reasoning about object-object interactions, by J.  The Noisy Brain: Stochastic Dynamics as a Principle of Call. Part II. Tool Use and Culture. A coming of age for Brain Function. E. T. Rolls & G. Deco. Oxford, U.K.: cultural panthropology, by A. Whiten; The cultural mind of Oxford University Press, 2010. 310 pp. [Price: £37.95] chimpanzees: How social tolerance can shape the transmis-  Quirks of Human Anatomy: An Evo-Devo Look at the sion of culture, by V. Horner; How are army ants shedding Human Body. L. I. Held, Jr. Cambridge, U.K.: Cambridge new light on culture in chimpanzees? by T. Humle; The University Press, 2009. 272 pp. [Price: £65.00] complexity of chimpanzee tool-use behaviors, by C. M. Sanz & D. B. Morgan; Tools, traditions, and technologies:  Saraguatos: Voces de la Selva. J. C. Serio Silva. Secre- Interdisciplinary approaches to chimpanzee nut cracking, taría de Educación de Veracruz, 2009. . wild chimpanzees, by M. Nakamura; and New theaters of  Wild Mammals in Captivity: Principles and Techniques conflict in the animal culture wars: Recent findings from for Zoo Management, 2nd ed. D. G. Kleiman, K. V. Thompson, & C. Kirk Baer (Eds.). University of Chicago   We would like to acknowledge Primate-Science as a source Press, 2010. for information about new books.

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Magazines and Newsletters keys in north-western Amazonia, by P. R. Stevenson & D. C. Guzmán-Caro; Pattern of maternal circulating CRH in  American Journal of Primatology, 2010, 72[8], laboratory-housed squirrel and owl monkeys, by M. L. . ers, & E. P. Zorrilla; Variation in physiological health of Contents: Personality in nonhuman primates: A review diademed sifakas across intact and fragmented forest at and evaluation of past research, by H. D. Freeman & S. D. Tsinjoarivo, eastern Madagascar, by M. T. Irwin, R. E. Gosling; Ovarian reserve tests and their utility in predicting Junge, J.-L. Raharison, & K. E. Samonds; and Variation in response to controlled ovarian stimulation in rhesus mon- dental wear and tooth loss among known-aged, older ring- keys, by J. M. Wu, D. L. Takahashi, D. K. Ingram, J. A. tailed lemurs (Lemur catta): A comparison between wild Mattison, G. Roth, M. A. Ottinger, & M. B. Zelinski; Time and captive individuals, by F. P. Cuozzo, M. L. Sauther, L. course of vocal modulation during isolation in common Gould, R. W. Sussman, L. M. Villers, & C. Lent. marmosets (Callithrix jacchus), by C. Yamaguchi, A. Izumi, & K. Nakamura; A longitudinal study of urinary  American Journal of Primatology, 2010, 72[12], dipstick parameters in wild chimpanzees (Pan troglodytes . E. Skjerve, T. Deschner, C. Boesch, J. Riedel, & F. H. Contents: Hunting strategies in wild common marmo- Leendertz; Phylogenetic analysis of the fecal flora of the sets are prey and age dependent, by N. Schiel, A. Souto, L. wild pygmy loris, by X. Bo, H. Zun-xi, W. Xiao-yan, G. Huber, & B. M. Bezerra; Phylogeny and distribution of Run-chi, T. Xiang-hua, M. Yue-lin, Y. Yun-Juan, S. Hui, crested gibbons (genus Nomascus) based on mitochondrial & Z. Li-da; Flexibility in the use of requesting gestures in cytochrome b gene sequence data, by Van Ngoc Thinh, B. squirrel monkeys (Saimiri sciureus), by J. R. Anderson, H. Rawson, C. Hallam, M. Kenyon, T. Nadler, L. Walter, & Kuroshima, Y. Hattori, & K. Fujita; Phylogeography of the C. Roos; The use of new world primates for biomedical Angolan black and white colobus monkey, Colobus ango- research: An overview of the last four decades, by L. Brito lesnsis palliatus, in Kenya and Tanzania, by M. M. Torres, B. H. Silva Araujo, P. H. Gomes de Castro, F. Ro- McDonald & H. Hamilton; Floating limb behaviors and mero Cabral, K. Sarges Marruaz, M. Silva Araujo, S. Go- self-biting are associated in laboratory monkeys, by K. L. mes da Silva, J. A. Pereira Carneiro Muniz, & E. Abrão Bentson, C. M. Crockett, K. L. Wahl, E. P. Runeson, R. U. Cavalheiro; Does nonnutritive tree gouging in a rainforest- Bellanca, G. H. Lee, J. P. Thom, H. B. Montgomery, M. H. dwelling lemur convey resource ownership as does loud Yi, J. G. S. McComas, & J. C. Ha; and Mating promiscuity calling in a dry forest-dwelling lemur? by S. Rasolohari- and reproductive tactics in female black and gold howler jaona, B. Randrianambinina, & M. Joly-Radko; Reproduc- monkeys (Alouatta caraya) inhabiting an island on the tive characteristics of wild female Phayre’s leaf monkeys, Parana river, Argentina, by M. M. Kowalewski & P. A. by A. Lu, C. Borries, N. M. Czekala, & J. C. Beehner; Garber. Specific gravity and creatinine as corrections for variation in urine concentration in humans, gorillas, and woolly  American Journal of Primatology, 2010, 72[11], monkeys, by B. C. White, K. M. Jamison, C. Grieb, D. . sleeping habits of the Yunnan snub-nosed monkey in Contents: Testing extraction and storage parameters for Xiangguqing, China, by D. Li, B. Ren, C. C. Grueter, B. a fecal hormone method, by D. J. Pappano, E. K. Roberts, Li, & M. Li; Line transect surveying of arboreal monkeys: & J. C. Beehner; Mated pairs of owl monkeys (Aotus Problems of group size and spread in a highly fragmented nancymaae) exhibit sex differences in response to unfamil- landscape, by S. F. Ferrari, R. R. D. Chagas, & J. Pedro iar male and female conspecifics, by C. K. Wolovich, S. Souza-Alves; Density and microhabitat use of Bengal slow Evans, & S. M. Green; Ape behavior in two alternating loris in primary forest and non-native plantation forest, by environments: Comparing exhibit and short-term holding M. Pliosungnoen, G. Gale, & T. Savini; Male dominance areas, by S. R. Ross, K. E. Wagner, S. J. Schapiro, & J. and reproductive success in wild white-faced capuchins Hau; The ontogeny of handling hard-to-process food in (Cebus capucinus) at Lomas Barbudal, Costa Rica, by L. wild brown capuchins (Cebus apella apella): Evidence Muniz, S. Perry, J. H. Manson, H. Gilkenson, J. Gros- from foraging on the fruit of Maximiliana maripa, by N. Louis, & L. Vigilant; and How many species of woolly Gunst, J.-B. Leca, S. Boinski, & D. Fragaszy; The commu- monkeys inhabit Colombian forests? By S. Botero, L. Y. nicative content of the common marmoset phee call during Rengifo, M. L. Bueno, & P. R. Stevenson. antiphonal calling, by C. T., Miller, K. Mandel, & X. Wang; Effects of food, proximity, and kinship on social behavior  Animal Behaviour, 2010, 80[1], . & R. W. Sussman; Nutrient transport within and between Contents include: The central importance of informa- habitats through seed dispersal processes by woolly mon- tion in studies of animal communication, by R. M. Sey-

19 Laboratory Primate Newsletter, 2011, 50[1]

farth, D. L. Cheney, T. Bergman, J. Fischer, K. Zuber- Linklater; Chimpanzee helping in collaborative and non- bühler, & K. Hammerschmidt; Ranging patterns of hama- collaborative contexts, by J. R. Greenberg, K. Hamann, F. dryas baboons: Random walk analyses, by A. L. Schreier Warneken, & M. Tomasello; Individual variation in tempo- & M. Grove; Message ‘scent’: Lemurs detect the genetic ral activity patterns in open-field tests, by P.-O. Montiglio, relatedness and quality of conspecifics via olfactory cues, D. Garant, D. Thomas, & D. Réale; and Comparing sam- by M. J. E. Charpentier, J. C. Crawford, M. Boulet, & C. ples with large numbers of zeros, by G. D. Ruxton, D. Rey, M. Drea; What time is it? Coping with expected feeding & M. Neuhäuser. time in capuchin monkeys, by E. Polizzi di Sorrentino, G. Schino, E. Visalberghi, & F. Aureli; and Spatial reference  Animal Behaviour, 2010, 80[6], . Egocentric or allocentric? By A. Presotto & P. Izar. Contents include: Inducing traditions in captive capuchin monkeys (Cebus apella), by J. Crast, J. M. Hardy, &  Animal Behaviour, 2010, 80[2], . try and physical attractiveness, by S. W. Gangestad, L. A. Contents include: Conflicts induce affiliative interac- Merriman, & M. E. Thompson; and A comparison of tions among bystanders in a tolerant species of macaque bonobo and chimpanzee tool use: Evidence for a female (Macaca tonkeana), by A. De Marco, R. Cozzolino, F. bias in the Pan lineage, by T. Gruber, Z. Clay, & K. Dessì-Fulgheri, & B. Thierry; How wild bearded capuchin Zuberbühler. monkeys select stones and nuts to minimize the number of strikes per nut cracked, by D. M. Fragaszy, R. Greenberg,  Brain, Behavior and Evolution, 2010, 76[2], E. Visalberghi, E. B. Ottoni, P. Izar, & Q. Liu; and Statis- . distributed in time using Ripley’s functions, by M. Mar- Contents include: Comparative brain collections are an coux, G. Larocque, M. Auger-Méthé, P. Dutilleul, & M. indispensable resource for evolutionary neurobiology, by M. Humphries. A. N. Iwaniuk; A voxel-based morphometry analysis of white matter asymmetries in chimpanzees (Pan troglo-  Animal Behaviour, 2010, 80[3], . Schenker, & C. C. Sherwood; and Extensive changes in the Contents include: Vocal greeting behaviour in wild expression of the opioid genes between humans and chim- chimpanzee females, by M. N. C. Laporte & K. Zuber- panzees, by P. Cruz-Gordillo, O. Fedrigo, G. A. Wray, & bühler; Does watching a monkey change its behaviour? C. C. Babbitt. Quantifying observer effects in habituated wild primates using automated radiotelemetry, by M. C. Crofoot, T. D.  Comparative Medicine, 2010, 60[5], . structing animal social networks from independent small- Contents include: Experimental induction of reduced group observations, by C. Perreault; Recognizing and re- ovarian reserve in a nonhuman primate model (Macaca specting claims over resources in free-ranging rhesus mon- fascicularis), by S. E. Appt, T. B. Clarkson, P. B. Hoyer, keys, Macaca mulatta, by B. E. Russ, J. A. Comins, R. N. D. Kock, A. K. Goode, C. M. May, J. T. Persyn, N. K. Smith, & M. D. Hauser; and Repeated measures analysis of Vail, K. F. Ethun, H. Chen, N. Sen, & J. R. Kaplan; Tho- contests and other dyadic interactions: Problems of seman- racic radiography as a refinement methodology for the tics, not statistical validity, by M. Briffa & R. W. Elwood. study of H1N1 influenza in cynomologus macaques (Macaca fascicularis), by D. L. Brining, J. S. Mattoon, L.  Animal Behaviour, 2010, 80[4], . J. Parnell; and Radiographic incidence of spinal osteopa- Contents include: Coalition formation among Barbary thologies in captive rhesus monkeys (Macaca mulatta), by macaque males: The influence of scramble competition, by B. Hernández-Godínez, A. Ibáñez-Contreras, G. Perdigón- A. Berghänel, O. Schülke, & J. Ostner; and Should risk Castañeda, A. Galván-Montaño, G. García-Montes de Oca, allocation strategies facilitate or hinder habituation to C. Zapata-Valdez, & E. Tena-Betancourt. nonlethal disturbance in wildlife? By E. Sirot.  Folia Primatologica, 2010, 81[3], . .com/science/journal/00033472>. Contents: Molecular systematics and phylogeography Contents include: Predator-deterring alarm call se- of the genus Lagothrix (Atelidae, Primates) by means of quences in Guereza colobus monkeys are meaningful to the mitochondrial COII gene, by M. Ruiz-Garcia & M. O. conspecifics, by A. M. Schel, A. Candiotti, & K. Zuber- Pinedo-Castro; Feeding ecology, food availability and bühler; No evidence for ovarian synchrony or asynchrony ranging patterns of wild Hamadryas baboons at Filoha, by in hamadryas baboons, by R. Tobler, S. Pledger, & W. A. L. Schreier; Evaluation of male inter-troop transfer as a

20 Laboratory Primate Newsletter, 2011, 50[1]

mating strategy among ring-tailed lemurs on St. Catherines Contents include: The colobus monkeys of Kenya; Island, USA, by J. A. Parga; and Play behavior of red Meet Rosie, the newest IPPL gibbon; Remembering Mar- colobus monkeys in Kibale National Park, Uganda, by E. jorie Doggestt; and announcements and requests for help. A. Worch.  Journal of the American Association for Laboratory  IDA–Africa – Fall eNews, Oct 5, 2010, . ida-africa.org>. Contents include: Measurement of fetal biparietal di- ameter in owl monkeys (Aotus nancymaae), by A. M.  International Journal of Primatology, 2010, 31[5], Schuler, A. G., Brady, G. W. Tustin, V. L. Parks, C. G. . Morris, & C. R. Abee; Multidimensional cost-benefit Contents: Functions of intermittent locomotion in mus- analysis to guide evidence-based environmental enrich- tached tamarins (Saguinus mystax), by M. Stojan-Dolar & ment: Providing bedding and foraging substrate to pen- E. W. Heymann; Rondon’s marmoset, Mico rondoni sp. n., housed monkeys, by A. J. Bennett, C. A. Corcoran, V. A. from southwestern Brazilian Amazonia, by S. F. Ferrari, L. Hardy, L. R. Miller, & P. J. Pierre; Population genetic Sena, M. P. C. Schneider, & J. S. Silva, Jr.; It’s all in the statistics from rhesus macaques (Macaca mulatta) in three timing: Birth seasonality and infant survival in Eulemur different housing configurations at the California National rubriventer, by S. R. Tecot; Asymmetry and dimensions of Primate Research Center, by S. Kanthaswamy, A. Kou, & relationship quality in the Japanese macaque (Macaca fus- D. G. Smith; A comprehensive laboratory animal facility cata yakui), by B. Majolo, R. Ventura, & G. Schino; Peru- pandemic response plan, by G. S. Roble, N. M. Lingenhol, vian red uakaris (Cacajao calvus ucayalii) are not flooded- B. Baker, A. Wilkerson, & R. J. Tolwani; and Nonsurgical forest specialists, by E. W. Heymann & R. Aquino; Vocal repair of a pseudoaneurysm in a cynomolgus macaque repertoire of golden-backed uakaris (Cacajao melano- (Macaca fascicularis), by J. S. Daviau & D. A. Merton. cephalus): Call structure and context, by B. Martins Bez- erra, A. S. Souto, & G. Jones; Levels of intraspecific varia-  Journal of the American Association for Laboratory tion within the catarrhine skeleton, by L. T. Buck, J. T. Animal Science, 2010, 49[6], . Stock, & R. A. Foley; Effects of habitat structure and Contents include: Pharmacokinetics of cefovecin in fragmentation on diversity and abundance of primates in squirrel monkey (Saimiri sciureus), rhesus macaques tropical deciduous forests in Bolivia, by L. W. Pyritz, A. B. (Macaca mulatta), and cynomolgus macaques (Macaca S. Büntge, S. K. Herzog, & M. Kessler; Genetic conse- fascicularis), by R. Papp, A. Popovic, N. Kelly, & R. quences of habitat fragmentation in black-and-gold howler Tschirret-Guth; Generation of a specific-pathogen-free (Alouatta caraya) populations from northern Argentina, by baboon colony, by R. F. Wolf, R. Eberle, & G. L. White; L. I. Oklander, M. M. Kowalewski, & D. Corach; Design Recurrent idiopathic gingival enlargement in an olive ba- and analysis of line transect surveys for primates, by S. T. boon (Papio anubis), by K. Kolappaswamy, S. Shipley, M. Buckland, A. J. Plumptre, L. Thomas, & E. A. Rexstad; A. Reynolds, C. McLeod, & L. Louis; Camptomelia in a Food sharing in lion tamarins (Leontopithecus chrysome- rhesus macaque (Macaca mulatta), by K. Hopper, P. las): Does foraging difficulty affect investment in young Morales, A. Garcia, & J. Wagner; Giant thoracic schwan- by breeders and helpers? by A. C. de A. Moura, H. G. noma in a rhesus macaque (Macaca mulatta), by D. A. Nunes, & A. Langguth; Exploring new areas: How impor- Alves, T. M. Bell, C. Benton, E. J. Rushing, & E. L. Ste- tant is long-term spatial memory for mangabey (Lophoce- vens; and Successful treatment of cryptosporidiosis in 2 bus albigena johnstonii) foraging efficiency? by K. R. L. common marmosets (Callithrix jacchus) by using Janmaat & R. L. Chancellor; Seasonal variations in the diet paromomycin, by N. E. Hahn & S. V. Capuano, III. and feeding effort of two groups of howlers in different  Journal of Medical Primatology, 2010, 39[5], sized forest fragments, by J. C. Dunn, J. Cristóbal- Azkarate, & J. J. Veà; Abundance and morphology of . Japanese macaques in snowy areas, by H. Enari & H. Sa- An updated review of simian betaretrovirus (SRV) in kamaki; and Gastrointestinal parasites of indigenous and macaque hosts, by N. A. Montiel; Epithelioid hemangioen- introduced primate species of Rubondo Island National dothelioma in the right auricle of an adult, male rhesus Park, Tanzania, by J. Petrášová, D. Modrý, M. A. Huff- macaque (Macaca mulatta), by E. D. Lombardini, R. Vir- man, M. I. Mapua, L. Bobáková, V. Mazoch, J. Singh, T. mani, T. W. Blanchard, J. F. Lafond, S. Ménard, & M. Kaur, and K. J. Petrželková. Doré; Evaluation of miosis, behavior and cholinesterase inhibition from low-level, whole-body vapor exposure to  IPPL News, September, 2010, 37[2], . (Intl Primate Protection League, P.O. R. F. Genovese, B. J. Benton, J. L. Oubre, P. J. Fleming, E. Box 766, Summerville, SC 29484 [e-mail: [email protected]]). M. Jakubowski, & R. J. Mioduszewski; Medical and surgi- cal management of reproductive neoplasia in two western lowland gorillas (Gorilla gorilla gorilla), by E. M.

21 Laboratory Primate Newsletter, 2011, 50[1]

Stringer, R. S. De Voe, F. Valea, S. Toma, G. Mulvaney, Population genetic parameter estimates for six populations A. Pruitt, B. Troan, & M. R. Loomis; Tetraparesis resem- of crowned lemurs, Eulemur coronatus (Gray, 1842), from bling acute transverse myelitis in a captive chimpanzee northern Madagascar, by R. Ramanamahefa, S. M. (Pan troglodytes): Long-term care and recovery, by T. Mi- McGuire, E. E. Louis, Jr., & R. A. Brenneman; Population yabe-Nishiwaki, A. Kaneko, K. Nishiwaki, A. Watanabe, genetic parameter estimates for five populations of San- S. Watanabe, N. Maeda, K. Kumazaki, M. Morimoto, R. ford’s lemur, Eulemur sanfordi (Archbold, 1932), from Hirokawa, J. Suzuki, Y. Ito, M. Hayashi, M. Tanaka, M. northern Madagascar, by R. Ramanamahefa, S. M. Tomonaga, & T. Matsuzawa; Leptin associations with age, McGuire, E. E. Louis, Jr., & R. A. Brenneman; Re- weight, and sex among chimpanzees (Pan troglodytes), by introduction of diademed sifaka (Propithecus diadema) R. G. Bribiescas & S. F. Anestis; and AIDS and optic neu- and black and white ruffed lemurs (Varecia variegata edi- ritis in a rhesus monkey infected with the R5 clade C torum) at Analamazaotra Special Reserve, Eastern Mada- SHIV-1157ipd3N4, by A. García, N. B. Siddappa, Q. Li, gascar, by S. R. Day, R. E. A. F. Ramarokoto, B. D. Sitz- A. T. Haase, K. Paul, F. Stroud, X. Zhang, J. A. Fountain, mann, R. Randriamboahanginjatovo, H. Ramanankirija, V. F. Villinger, F. J. Novembre, J. G. Else, W. E. Secor, & R. R. A. Randrianindrina, G. Ravololonarivo, & E. E. Louis, M. Ruprecht. Jr.; Distribution of a conservation-based activity book at two primary schools near Analamazaotra Special Reserve,  Journal of Medical Primatology, 2010, 39[6], Madagascar, by S. M. McGuire, B. D. Sitzmann, K. . Louis, Jr.; Population survey of the Greater bamboo lemur Estimates of milk constituents from lactating bonnet (Prolemur simus) at Kianjavato Classified Forest, by S. M. macaque (Macaca radiata) mothers between two and McGuire, C. A. Bailey, J.-N. Rakotonirina, L. G. Razana- seven months post-partum, by M. L. Laudenslager, C. Nat- jatovo, J. F. Ranaivoarisoa, L. M. Kimmel, & E. E. Louis, vig, H. Cantwell, M. C. Neville, & M. L. Reite; Frequency Jr.; Impact du tourisme sur Prolemur simus à Talatakely, of the major histocompatibility complex Mamu-A*01 allele dans le Parc National de Ranomafana, by J. A. Norosoari- in experimental rhesus macaques in China, by W. Wang, naivo, C. Tan, L. Rabetafika, & D. Rakotondravony; Pos- Z. Cong, X. Liu, W. Tong, H. Qiao, H. Jiang, Q. Wei, & C. sible new Mirza taxon from the Fiherenana River valley, Qin; Urinary estrogens, progesterone, and LH changes Atsimo-Andrefana Region, by C. J. Gardner & L. Jasper; during normal menstrual cycles of a captive female Rapid primatological surveys of the Andringitra forest cor- pileated gibbon (Hylobates pileatus), by Y. Aramaki, H. ridors: Direct observation of the greater bamboo lemur Oae, Y. Mouri, K. Takizawa, K. Nakanishi, Y. Hyoudou, (Prolemur simus), by K. E. Delmore, M. F. Keller, E. E. M. Omasa, & H. Kusunoki; Splenic angioleiomyoma in an Louis, Jr., & S. E. Johnson; Allomothering and allonursing owl monkey (Aotus nancymae), by A. S. Gozalo, P. M. behaviour in collared lemurs (Eulemur collaris), by K. Zerfas, M. F. Starost, W. R. Elkins, & C. L. Clarke; Clini- Kesch; Costs of alarm calling: Lemur alarm calls attract cal chemistry and hematology values in a Caribbean popu- fossas, by C. Fichtel; Involving local communities in con- lation of African green monkeys, by S. Liddie, R. J. servation: An example involving blue-eyed black lemurs Goody, R. Valles, & M. S. Lawrence; Real-time telemetric 60 (Eulemur flavifrons), by M. S. N. Volampeno & C. T. monitoring in whole-body Co gamma-photon irradiated Downs; Funding and training; and Theses completed. rhesus macaques (Macaca mulatta), by C. A. Carrier, T. B. Elliott, & G. D. Ledney; Retrospective case-control study  Primate Conservation, Inc. UPDATE, 2010, of hyperglycemia in group-housed, mature female cyno- . (1411 Shannock Rd, molgus macaques (Macaca fascicularis), by S. A. Bauer, Charlestown, RI 02813-3726). K. E. Leslie, D. L. Pearl, J. Fournier, & P. V. Turner; Isola- tion, identification of Streptococcus pneumoniae from in-  Primates, 2010, 51[4], . Luo, Z. Chen, A. Cheng, M. Wang, D. Zhu, R. Jia, F. Liu, Contents: Observed infanticides following a male im- X. Chen, Y. Zhou, F. Bi, & Z. Yang. migration event in black howler monkeys, Alouatta pigra, at Palenque National Park, Mexico, by S. Van Belle, A. E.  Lemur News: The Newsletter of the Madagascar Section Kulp, R. Thiessen-Bock, M. García, & A. Estrada; Identi- of the IUCN/SSC Primate Specialist Group, December, fication of non-taster Japanese macaques for a specific 2009, No. 14, . bitter taste, by N. Suzuki, T. Sugawara, A. Matsui, Y. Go, Contents: Rapid lemur survey in northern Menabe, by & H. Hirai; Theropithecus gelada distribution and varia- M. Dammhahn, L. Schäffler, C. Fichtel, & P. M. Kappeler; tions related to taxonomy: History, challenges and implica- Grazing lemurs: Exhibition of terrestrial feeding by the tions for conservation, by S. Gippoliti; Aggression does not southern gentle lemur, Hapalemur meridionalis, in the increase friendly contacts among bystanders in geladas Mandena littoral forest, southeast Madagascar, by T. M. (Theropithecus gelada), by A. Leone, M. Mignini, G. Eppley & G. Donati; Note on lemurs of the Réserve Spé- Mancini, and E. Palagi; Polyspecific associations of Cer- ciale d’Ambohitantely, Madagascar, by J. M. Ralison; copithecus campbelli and C. petaurista with C. diana:

22 Laboratory Primate Newsletter, 2011, 50[1]

What are the costs and benefits? by P. J. Buzzard; Maternal serves in the ethical training of primatologists, by P. A. care and infant development in Callimico goeldii and Cal- Garber, A. Molina, & R. L. Molina; Male mating tactics in lithrix jacchus, by A. C. Ross, L. M. Porter, M. L. Power, spider monkeys: Sneaking to compete, by K. N. Gibson; & V. Sodaro; Responses of golden-backed uakaris, Caca- Preliminary evidence of accumulation of stress during jao melanocephalus, to call playback: Implications for sur- translocation in mantled howlers, by M. A. Socorro Agui- veys in the flooded Igapó forest, by B. M. Bezerra, A. S. lar-Cucurachi, P. A. D. Dias, A. Rangel-Negrín, R. Souto, & G. Jones; Two-year-old children copy more re- Chavira, L. Boeck, & D. Canales-Espinosa; Estimates of liably and more often than nonhuman great apes in multi- heritability for reproductive traits in captive rhesus ma- ple observational learning tasks, by C. Tennie, K. Greve, caque females, by C. Gagliardi, K. P. Falkenstein, D. E. H. Gretscher, & J. Call; Host age, sex, and reproductive Franke, & H. M. Kubisch; and Feeding ecology of Bornean seasonality affect nematode parasitism in wild Japanese orangutans (Pongo pygmaeus morio) in Danum Valley, macaques, by A. J. J. MacIntosh, A. D. Hernandez, & M. Sabah, Malaysia: A 3-year record including two mast fruit- A. Huffman; and The Primates 2010 Most-Cited Paper ings, by T. Kanamori, N. Kuze, H. Bernard, T. P. Malim, Award is conferred upon Dr. Satoshi Hirata. & S. Kohshima.

 Research Saves, 2010, Issue 3, . com/doi/10.1002/ajp.v72:10/issuetoc>. Contents: The ethnoprimatological approach in prima-  Zoo Biology, 2010, 29[4], < onlinelibrary.wiley. tology, by A. Fuentes & K. J. Hockings; Macaques in >. com/doi/10.1002/zoo.v29:4/issuetoc farms and folklore: Exploring the human–nonhuman pri- Contents include: Observational methods to measure mate interface in Sulawesi, Indonesia, by E. P. Riley & N. behaviors of captive cotton-top tamarins (Saguinus oedi- E. C. Priston; Human–nonhuman primate interactions pus), by L. N. Edwards, A. E. Sorkin, R. C. Rhodes, III, & amongst Tikuna people: Perceptions and local initiatives K. H. Petersson; and Female reproductive parameters in for resource management in Amacayacu in the Colombian the Javan gibbon (Hylobates moloch), by S. Hodgkiss, E. Amazon, by H. E. Parathian & A. M. Maldonado; Local Thetford, C. D. Waitt, & V. Nijman. attitudes and perceptions toward crop-raiding by orangu-  Zoo Biology, 2010, 29[5], . ern Sumatra, Indonesia, by G. Campbell-Smith, H. V. P. Contents include: Factors influencing weight changes Simanjorang, N. Leader-Williams, & M. Linkie; Exploring in callitrichids at the Bronx Zoo, by E. Kaplan & N. cultural drivers for wildlife trade via an ethnoprimatologi- Shelmidine; and The potential for microchip-automated cal approach: A case study of slender and slow lorises technology to improve enrichment practices, by J. M. Hoy, (Loris and Nycticebus) in South and Southeast Asia, by K. P. J. Murray, & A. Tribe. A. I. Nekaris, C. R. Shepherd, C. R. Starr, & V. Nijman; Attacks on local persons by chimpanzees in Bossou, Re- Proceedings public of Guinea: Long-term perspectives, by K. J. Hock-  Program and Abstracts of the 33rd Annual Meeting of the ings, G. Yamakoshi, A. Kabasawa, & T. Matsuzawa; Be- American Society of Primatologists, June 16–19, 2010. havioral responses of one western lowland gorilla (Gorilla American Journal of Primatology, 2010, 72[S1], gorilla gorilla) group at Bai Hokou, Central African Re- public, to tourists, researchers and trackers, by M. . sponses to researchers in a disturbed forest–farm mosaic at Special Journal Issues Bulindi, western Uganda, by M. R. McLennan & C. M. Hill; and Perceptions of nonhuman primates in human–  Special Section on Ethical Issues in Field Primatology. wildlife conflict scenarios, by C. M. Hill & A. D. Webber. American Journal of Primatology, 2010, 72[9], . 9, 2010. Contents: Field primatology of today: Current ethical Contents: Animal research: Why we need alternatives, issues, by K. C. MacKinnon & E. P. Riley; Ethical issues by H. Ferdowsian; Animal research: Groupthink in both faced by field primatologists: Asking the relevant ques- camps, by L. A. Hansen; and Animal Research: Activists’ tions, by L. M. Fedigan; Long-term field studies: Positive wishful thinking, primitive reasoning, by E. Holland. impacts and unintended consequences, by K. B. Strier;  One Health: The Intersection of Humans, Animals, and Ethics commentary: Subjects of knowledge and control in the Environment. ILAR Journal: Institute for Laboratory field primatology, by N. M. Malone, A. Fuentes, & F. J. Animal Research, 2010, 51[3], < White; Putting the community back in community ecology dels-old.nas.edu/ and education: The role of field schools and private re- ilar_n/ilarjournal/51_3/html>.

23 Laboratory Primate Newsletter, 2011, 50[1]

 Building Bridges Toward a New Understanding of Tar- with its number of nonneuronal cells, which is expected to sier Diversity. M. Shekelle & S. Gursky (Eds.). Interna- be proportional to the total length of myelinated axons in tional Journal of Primatology, 2010, 31[6], the white matter. This result implies that the average ax- . onal cross-section area in the white matter, a, does not Contents: Why tarsiers? Why now? An introduction to scale significantly with the number of neurons in the gray the special edition on tarsiers, by M. Shekelle & S. Gursky; matter, N. The surface area of the white matter increases Progreditur ordinara saltando et retrorsum...Normally with N0.87, not N1.0. Because this surface can be defined as proceeds in a leaping fashion, and backwards..., by C. T. the product of N, a, and the fraction n of cortical neurons Niemitz; Vertical clinging and leaping revisited: Locomo- connected through the white matter, we deduce that con- tion and habitat use in the western tarsier, Tarsius ban- nectivity decreases in larger cerebral cortices as a slowly canus explored via loglinear modeling, by R. H. Crompton, diminishing fraction of neurons (which varies with N–0.16) M. L. Blanchard, S. Coward, R. McNeill Alexander, & S. sends myelinated axons into the white matter. Decreased K. Thorpe; Influence of orbit size on aspects of the tarsier connectivity is compatible with previous suggestions that postorbital septum, by D. G. Savakova & M. Dagosto; neurons in the cerebral cortex are connected as a small- Overview of sensory systems of Tarsius, by P. Wong, C. world network and should slow down the increase in E. Collins & J. H. Kaas; The skull of Tarsius: Functional global conduction delay in cortices with larger numbers of morphology, eyeballs, and the nonpursuit predatory life- neurons. Further, a simple model shows that connectivity style, by A. L. Rosenberger; The rediscovery of Buffon’s and cortical folding are directly related across species. We tarsier, by C. Callou, J. Cuisin, & C. Groves; The genera offer a white matter-based mechanism to account for in- and species of Tarsiidae, by C. Groves & M. Shekelle; creased cortical folding across species, which we propose Molecular phylogenetics and chronometrics of Tarsiidae to be driven by connectivity-related tension in the white based on 12S mtDNA haplotypes: Evidence for Miocene matter, pulling down on the gray matter.” origins of crown tarsiers and numerous species within the  Functional organization for color and orientation in ma- Sulawesian clade, by M. Shekelle, R. Meier, I. Wahyu, caque V4. Tanigawa, H., Lu, H. D., & Roe, A. W. (Dept Wirdateti, & N. Ting; Tarsius wallacei: A new tarsier spe- of Psychology, Vanderbilt Univ., Nashville, TN 37203 [e- cies from central Sulawesi occupies a discontinuous range, mail: [email protected]]). Nature Neuroscience, by S. Merker, C. Driller, H. Dahruddin, Wirdateti, W. Si- 2010, 13, 1542-1548, < naga, D. Perwitasari-Farajallah, & M. Shekelle; Geo- www.nature.com/neuro/ >. graphical variation in duet songs of Sulawesi tarsiers: Evi- journal/v13/n12/full/nn.2676.html dence for new cryptic species in south and southeast Su- “Visual area V4 in the macaque monkey is a cortical lawesi, by J. A. Burton & A. Nietsch; Checkerboard pat- area that is strongly involved in color and shape percep- terns, interspecific competition, and extinction: Lessons tion. However, fundamental questions about V4 are still from distribution patterns of tarsiers (Tarsius) and slow debated. V4 was initially characterized as a color- lorises (Nycticebus) in insular Southeast Asia, by V. Ni- processing area, but subsequent studies revealed that it jman & K. A. I. Nekaris; Intraspecific variation in the mat- contains a diverse complement of cells, including those ing system of spectral tarsiers, by S. Gursky-Doyen; pre- with preference for color, orientation, disparity and higher- liminary data on the behavior, ecology, and morphology of order feature preferences. This has led to disputes and pygmy tarsiers (Tarsius pumilus), by N. Grow & S. Gur- uncertainty about the role of V4 in vision. Using intrinsic sky-Doyen; and Strengths and weaknesses of a population signal optical imaging methods in awake, behaving mon- viability analysis for Philippine tarsiers (Tarsius syrichta), keys, we found that different feature preferences are func- by I. Neri-Arboleda. tionally organized in V4. Optical images revealed that regions with preferential response to color were largely Anatomy and Physiology separate from orientation-selective regions. Our results  Connectivity-driven white matter scaling and folding in help to resolve long-standing controversies regarding func- primate cerebral cortex. Herculano-Houzel, S., Mota, B., tional diversity and retinotopy in V4 and indicate the pres- Wong, P., & Kaas, J. H. (J. H. K., Dept of Psych., Vander- ence of spatially biased distribution of featural representa- bilt Univ., Nashville, TN 37204 [e-mail: jon.h.kaas tion in V4 in the ventral visual pathway.” @vanderbilt.edu]). Proceedings of the National Academy  Separate value comparison and learning mechanisms in of Sciences, U.S.A., 2010, 107, 19008-19013, macaque medial and lateral orbitofrontal cortex. Noonan, . M. P., Walton, M. E., Behrens, T. E. J., Sallet, J., Buckley, “Larger brains have an increasingly folded cerebral M. J., & Rushworth, M. F. S. (Dept of Exp. Psych., Univ. cortex whose white matter scales up faster than the gray of Oxford, Oxford OX1 3UD, U.K. [e-mail: mary- matter. Here we analyze the cellular composition of the [email protected]]). Proceedings of the National subcortical white matter in 11 primate species, including Academy of Sciences, U.S.A., 2010, 107, 20547-20552, humans, and one Scandentia [tree shrew], and show that . the mass of the white matter scales linearly across species

24 Laboratory Primate Newsletter, 2011, 50[1]

“Uncertainty about the function of orbitofrontal cortex Zhu, X., Afanassieff, M., Savatier, P., Zhang, K., Zhou, Q., (OFC) in guiding decision-making may be a result of its & Ji, W. (W. J., Kunming Primate Res. Ctr, Chinese Acad. medial (mOFC) and lateral (lOFC) divisions having dis- of Sciences, Kunming 650223, P. R. China [e-mail: tinct functions. Here we test the hypothesis that the mOFC [email protected]]). Proceedings of the National Acad- is more concerned with reward-guided decision making, in emy of Sciences, U.S.A., 2010, 107, 17663-17667, contrast with the lOFC’s role in reward-guided learning. . Macaques performed three-armed bandit tasks and the ef- “The development of transgenic technologies in mon- fects of selective mOFC lesions were contrasted against keys is important for creating valuable animal models of lOFC lesions. First, we present analyses that make it pos- human physiology so that the etiology of diseases can be sible to measure reward-credit assignment—a crucial com- studied and potential therapies for their amelioration may ponent of reward-value learning—independently of the be developed. However, the efficiency of producing trans- decisions animals make. The mOFC lesions do not lead to genic primate animals is presently very low, and there are impairments in reward-credit assignment that are seen after few reports of success. We have developed an improved lOFC lesions. Second, we examined how the reward val- methodology for the production of transgenic rhesus mon- ues of choice options were compared. We present three keys, making use of a simian immunodeficiency virus analyses, one of which examines reward-guided decision (SIV)-based vector that encodes EGFP and a protocol for making independently of reward-value learning. Lesions infection of early-cleavage-stage embryos. We show that of the mOFC, but not the lOFC, disrupted reward-guided infection does not alter embryo development. Moreover, decision making. Impairments after mOFC lesions were a the timing of infection, either before or during embryonic function of the multiple option contexts in which decisions genome activation, has no observable effect on the level were made. Contrary to axiomatic assumptions of decision and stability of transgene expression. Of 70 embryos in- theory, the mOFC-lesioned animals’ value comparisons jected with concentrated virus at the one- to two-cell stage were no longer independent of irrelevant alternatives.” or the four- to eight-cell stage and showing fluorescence, 30 were transferred to surrogate mothers. One transgenic Animal Models fetus was obtained from a fraternal triple pregnancy. Four  PIB binding in aged primate brain: Enrichment of high- infant monkeys were produced from four singleton preg- affinity sites in humans with Alzheimer’s disease. Rosen, nancies, of which two expressed EGFP throughout the R. F., Walker, L. C., & LeVine, H., III. (L. C. W., Div. of whole body. These results demonstrate the usefulness of Neuroscience, Yerkes NPRC, Emory Univ., Atlanta, SIV-based lentiviral vectors for the generation of trans- GA 30322 [e-mail: [email protected]]). genic monkeys and improve the efficiency of transgenic Neurobiology of Aging, 2009, 32, 223-234, technology in nonhuman primates.” .  Extensive spontaneous plasticity of corticospinal projec- “Aged nonhuman primates accumulate large amounts tions after primate spinal cord injury. Rosenzweig, E. S., of human-sequence amyloid ß (Aß) in the brain, yet they Courtine, G., Jindrich, D. L., Brock, J. H., Ferguson, A. R., do not manifest the full phenotype of Alzheimer’s disease Strand, S. C., Nout, Y. S., Roy, R. R., Miller, D. M., (AD). To assess the biophysical properties of Aß that Beattie, M. S., Havton, L. A., Bresnahan, J. C., Edgerton, might govern its pathogenic potential in humans and non- V. R., & Tuszynskimtuszynski, M. H. (M. H. T., Dept of human primates, we incubated the benzothiazole imaging Neurosciences, U.C. San Diego, La Jolla, CA 92093 [e- agent Pittsburgh Compound B (PIB) with cortical tissue mail: [email protected]]. Nature Neurosci- homogenates from normal aged humans, humans with AD, ence, 2010, 13, 1505-1510, . chimpanzees with cerebral Aß-amyloidosis. Relative to “Although axonal regeneration after CNS injury is lim- humans with AD, high-affinity PIB binding is markedly ited, partial injury is frequently accompanied by extensive reduced in cortical extracts from aged nonhuman primates functional recovery. To investigate mechanisms underly- containing levels of insoluble Aß similar to those in AD. ing spontaneous recovery after incomplete spinal cord in- The high-affinity binding of PIB may be selective for a jury, we administered C7 spinal cord hemisections to adult pathologic, human-specific conformation of multimeric rhesus monkeys and analyzed behavioral, electrophysio- Aß, and thus could be a useful experimental tool for clari- logical and anatomical adaptations. We found marked fying the unique predisposition of humans to Alzheimer’s spontaneous plasticity of corticospinal projections, with disease.” reconstitution of fully 60% of pre-lesion axon density aris-  Transgenic rhesus monkeys produced by gene transfer ing from sprouting of spinal cord midline-crossing axons. into early-cleavage-stage embryos using a simian immuno- This extensive anatomical recovery was associated with deficiency virus-based vector. Niu, Y., Yu, Y., Bernat, A., improvement in coordinated muscle recruitment, hand Yang, S., He, X., Guo, X., Chen, D., Chen, Y., Ji, S., Si, function and locomotion. These findings identify what W., Lv, Y., Tan, T., Wei, Q., Wang, H., Shi, L., Guan, J., may be the most extensive natural recovery of mammalian

25 Laboratory Primate Newsletter, 2011, 50[1]

axonal projections after nervous system injury observed to rewards of similar magnitudes. Although such devaluation date, highlighting an important role for primate models in of delayed rewards has been almost universally described translational disease research.” by hyperbolic discount functions, the rate of this temporal Animal Welfare discounting varies substantially among different animal species. This might be in part due to the differences in  Pool deemed positive for primates. AWI Quarterly, 2010, how the information about reward is presented to decision 59[3], 21, . nitudes were gradually adjusted across trials, so the ani- Providing monkeys with “swimming pools” during the mals learned the properties of future rewards from the re- hot summer months is probably one of the most attractive wards they waited for and consumed previously. In con- environmental enrichments for them. Macaques and ba- trast, verbal cues have been used commonly in human boons are good swimmers and divers, but simply playing studies. In the present study, rhesus monkeys were trained with water can fascinate primates for long periods of time. in a novel inter-temporal choice task in which the magni-  Refinement of the use of food and fluid control as moti- tude and delay of reward were indicated symbolically us- vational tools for macaques used in behavioural neurosci- ing visual cues and varied randomly across trials. We ence research: Report of a working group of the NC3Rs. found that monkeys could extract the information about Prescott, M. J., Brown, V. J,, Flecknell, P. A., Gaffan, D., reward delays from visual symbols regardless of the num- Garrod, K., Lemon, R. N., Parker, A. J., Ryder, K., ber of symbols used to indicate the delay. The rate of tem- Schultz, W., Scott, L., Watson, J., & Whitfield, L. (NC3Rs, poral discounting observed in the present study was com- 20 Park Crescent, London W1B 1AL, U.K. [e-mail: parable to the previous estimates in other mammals, and [email protected]]). Journal of Neuroscience the animal’s choice behavior was largely consistent with Methods, 2010, 193, 167-188, hyperbolic discounting. Our results also suggest that the . rate of temporal discounting might be influenced by con- This report provides practical guidance on refinement textual factors, such as the novelty of the task. The flexi- of the use of food and fluid control as motivational tools bility furnished by this new inter-temporal choice task for macaques used in behavioral neuroscience research. might be useful for future neurobiological investigations The guidance is based on consideration of the scientific on inter-temporal choice in nonhuman primates.” literature and, where data are lacking, expert opinion and Care professional experience, including that of the members of a Working Group convened by the United Kingdom Na-  Case Report: Bilateral phacoemulsification in an orangu- tional Centre for the Replacement, Refinement and Reduc- tan (Pongo pygmaeus). Montiani-Ferreira, F., Lima, L., tion of Animals in Research (NC3Rs). The report should Bacellar, M., D’Otaviano Vilani, R. G., Fedullo, J. D., & be useful to researchers, veterinarians and animal care staff Lange, R. R. (Universidade Federal do Paraná (UFPR), responsible for the welfare of macaques used in food and Rua dos Funcionários, 1540, 80035-050, Curitiba, PR, fluid control protocols, as well as those involved with de- Brazil [e-mail: [email protected]]). Veterinary Ophthal- signing, performing and analyzing studies that use these mology, 2010, 13[Suppl. s1], 91-99, . animal care and use committees concerned with evaluating A 14-year-old, female, captive-born orangutan (Pongo such protocols. The report provides a framework for re- pygmaeus) developed bilateral cataracts. Ultrasonography, finement that can be tailored to meet local requirements. It electroretinography, and cataract correction using phacoe- also identifies data gaps and areas for future research and mulsification were performed bilaterally. This case report sets out the Working Group’s recommendations on con- aims to describe the ophthalmic procedures performed in temporary best practice. this animal critically endangered of extinction. The surgery successfully restored vision and normal activity to the Behavior patient.  Temporal discounting and inter-temporal choice in Conservation rhesus monkeys. Hwang, J., Kim, S., & Lee, D. (D. L., Dept of Neurobiol., Yale Univ. Sch. of Med., 333 Cedar  Being Jane Goodall. D. Quammen. National Geo- St, New Haven, CT 06510 [e-mail: daeyeol.lee@ graphic, October, 2010, . 2009, 3[9], . , photos from National leading to an immediate reward than actions with delayed

26 Laboratory Primate Newsletter, 2011, 50[1]

Geographic articles by and about her, and articles chondrial sequences, human P. falciparum formed a mo- . nophyletic lineage within the gorilla parasite radiation. These findings indicate that P. falciparum is of gorilla ori- Disease gin and not of chimpanzee, bonobo, or ancient human ori-  Island biogeography reveals the deep history of SIV. gin.” Worobey, M., Telfer, P., Souquière, S., Hunter, M., Cole-  Identification of a receptor for an extinct virus. Soll, S. J., man, C. A., Metzger, M. J., Reed, P., Makuwa, M., Hearn, Neil, S. J. D., & Bieniasz, P. D. (P. D. B., Aaron Diamond G., Honarvar, S., Roques, P., Apetrei, C., Kazanji, M., & AIDS Research Ctr, Rockefeller Univ., New York, NY Marx, P. A. (P. A. M., Tulane NPRC, Covington, LA 10016 [e-mail: [email protected]]). Proceedings of the 70433 [e-mail: [email protected]]). Science, 2010, 329, National Academy of Sciences, U.S.A., 2010, 107, 19496- 1487, . sci;329/5998/1487 >. “Simian immunodeficiency virus (SIV) lineages have long “The resurrection of endogenous retroviruses from in- been identified that are endemic to Bioko Island. The time active molecular fossils has allowed the investigation of the island formed offers a geological time scale calibration interactions between extinct pathogens and their hosts that point for dating the most recent common ancestor of SIV. occurred millions of years ago. Two such paleoviruses, The Bioko viruses cover the whole range of SIV genetic chimpanzee endogenous retrovirus-1 and -2 (CERV1 and diversity, and each Bioko SIV clade is most closely related CERV2), are relatives of modern MLVs and are found in to viruses circulating in hosts of the same genus on the the genomes of a variety of Old World primates, but are African mainland rather than to SIVs of other Bioko spe- absent from the human genome. No extant CERV1 and -2 cies. Our phylogeographic approach establishes that SIV proviruses are known to encode functional proteins. To is ancient and at least 32,000 years old. Our conservative investigate the host range restriction of these viruses, we calibration point and analyses of gene sequence saturation attempted to reconstruct functional envelopes by generat- and dating bias suggest it may be much older.” ing consensus genes and proteins. CERV1 and -2 envel-  Origin of the human malaria parasite Plasmodium falci- oped MLV particles infected cell lines from a range of parum in gorillas. Liu, W., Li, Y., Learn, G. H., Rudi- mammalian species. Using CERV2 Env-pseudotyped cell, R. S., Robertson, J. D., Keele, B. F., Ndjango, J.-B. MLV reporters, we identified copper transport protein 1 N., Sanz, C. M., Morgan, D. B., Locatelli, S., Gonder, M. (CTR1) as a receptor that was presumably used by CERV2 K., Kranzusch, P. J., Walsh, P. D., Delaporte, E., Mpoudi- during its ancient exogenous replication in primates. Ex- Ngole, E., Georgiev, A. V., Muller, M. N., Shaw, G. M., pression of human CTR1 was sufficient to confer CERV2 Peeters, M., Sharp, P. M., Rayner, J. C., & Hahn, B. H. (B. permissiveness on otherwise resistant hamster cells, and H. H., Dept of Med., Univ. of Alabama, Birmingham, AL CTR1 knockdown or CuCl2 treatment specifically inhib- 35294 [e-mail: [email protected]]). Nature, 2010, 467, ited CERV2 infection of human cells. Mutations in highly 420-425, . resistant to CERV2 include a unique deletion in a copper- “Plasmodium falciparum is the most prevalent and le- binding motif. These CERV2 receptor-inactivating muta- thal of the malaria parasites infecting humans, yet the ori- tions in hamster CTR1 are accompanied by apparently gin and evolutionary history of this important pathogen compensating changes, including an increased number of remain controversial. Here we develop a single-genome extracellular copper-coordinating residues, and this may amplification strategy to identify and characterize Plasmo- represent an evolutionary barrier to the acquisition of dium spp. DNA sequences in fecal samples from wild- CERV2 resistance in primates.” living apes. Among nearly 3,000 specimens collected from  Advanced antisense therapies for postexposure protection field sites throughout central Africa, we found Plasmodium against lethal filovirus infections. Warren, T. K., War- infection in chimpanzees (Pan troglodytes) and western field, K. L., Wells, J., Swenson, D. L., Donner, K. S., Van gorillas (Gorilla gorilla), but not in eastern gorillas (Go- Tongeren, S. A., Garza, N. L., Dong, L., Mourich, D. V., rilla beringei) or bonobos (Pan paniscus). Ape plasmodial Crumley, S., Nichols, D. K., Iversen, P. L., & Bavari, S. infections were highly prevalent, widely distributed, and (S. B., USAMRIID, Fort Detrick, MD 21702-9255 [e-mail: almost always made up of mixed parasite species. Analy- [email protected]]). Nature Medicine, 2010, sis of more than 1,100 mitochondrial, apicoplast, and nu- 16, 991-994, < clear gene sequences from chimpanzees and gorillas re- www.nature.com/nm/journal/v16/n9/ vealed that 99% grouped within one of six host-specific full/nm.2202.html>. lineages representing distinct Plasmodium species within “Currently, no vaccines or therapeutics are licensed to the subgenus Laverania. One of these from western goril- counter Ebola or Marburg viruses, highly pathogenic las comprised parasites that were nearly identical to P. fal- filoviruses that are causative agents of viral hemorrhagic ciparum. In phylogenetic analyses of full-length mito- fever. Here we show that administration of positively charged phosphorodiamidate morpholino oligomers

27 Laboratory Primate Newsletter, 2011, 50[1]

(PMOplus), delivered by various dosing strategies initiated 1/3. This relationship suggests that the extension, mass 30–60 min after infection, protects >60% of rhesus mon- and number of neurons that compose the spinal cord are keys against lethal Zaire Ebola virus (ZEBOV) and 100% related to body length, rather than to body mass or surface. of cynomolgus monkeys against Lake Victoria Marburg Moreover, we show that although brain mass increases virus (MARV) infection. PMOplus may be useful for linearly with cord mass, the number of neurons in the brain treating these and other highly pathogenic viruses in hu- increases with the number of neurons in the spinal cord mans.” raised to the power of 1.7. This faster addition of neurons Evolution, Genetics, and Taxonomy to the brain than to the spinal cord is consistent with current views on how larger brains add complexity to the  Cellular scaling rules for the brains of an extended num- processing of environmental and somatic information.” ber of primate species. Gabi, M., Collins, C. E., Wong, P., Torres, L. B., Kaas, J. H., & Herculano-Houzel, S. (S. H.-  Rhesus monkeys (Macaca mulatta) do recognize them- H., Inst. de Ciências Bioméd., UFRJ, Av. Carlos Chagas selves in the mirror: Implications for the evolution of self- Filho, 373, Ilha do Fundão, Rio de Janeiro, RJ 21941-902, recognition. Rajala, A. Z., Reininger, K. R., Lancaster, K. Brazil [e-mail: [email protected]]). Brain, Behavior M., & Populin, L. C. (Dept of Psych., Univ. of Wisconsin, and Evolution, 2010, 76, 32-44. Madison, WI 53706 [e-mail: [email protected]]). PLoS “What are the rules relating the size of the brain and its ONE, 2010, 5[9], e12865, . their average sizes? We have shown previously that the “Self-recognition in front of a mirror is used as an indi- cerebral cortex, cerebellum and the remaining brain struc- cator of self-awareness. Along with humans, some chim- tures increase in size as a linear function of their numbers panzees and orangutans have been shown to be self-aware of neurons and non-neuronal cells across six species of using the mark test. Monkeys are conspicuously absent primates. Here we describe that the cellular composition from this list because they fail the mark test and show per- of the same brain structures of five other primate species, sistent signs of social responses to mirrors despite pro- as well as humans, conform to the scaling rules identified longed exposure, which has been interpreted as evidence of previously, and that the updated power functions for the a cognitive divide between hominoids and other species. extended sample are similar to those determined earlier. In stark contrast with those reports, the rhesus monkeys in Accounting for phylogenetic relatedness in the combined this study, who had been prepared for electrophysiological dataset does not affect the scaling slopes that apply to the recordings with a head implant, showed consistent self- cerebral cortex and cerebellum, but alters the slope for the directed behaviors in front of the mirror and showed social remaining brain structures to a value that is similar to that responses that subsided quickly during the first experimen- observed in rodents, which raises the possibility that the tal session. The self-directed behaviors, which were per- neuronal scaling rules for these structures are shared formed in front of the mirror and did not take place in its among rodents and primates. The conformity of the new absence, included extensive observation of the implant and set of primate species to the previous rules strongly sug- genital areas that cannot be observed directly without a gests that the cellular scaling rules we have identified ap- mirror. We hypothesize that the head implant, a most sali- ply to primates in general, including humans, and not only ent mark, prompted the monkeys to overcome gaze aver- to particular subgroups of primate species. In contrast, the sion inhibition or lack of interest in order to look and ex- allometric rules relating body and brain size are highly amine themselves in front of the mirror. The results of this sensitive to the particular species sampled, suggesting that study demonstrate that rhesus monkeys do recognize them- brain size is neither determined by body size nor together selves in the mirror and, therefore, have some form of self- with it, but is rather only loosely correlated with body awareness. Accordingly, instead of a cognitive divide, size.” they support the notion of an evolutionary continuity of mental functions.”  Cellular scaling rules for primate spinal cords. Burish, M. J., Peebles, J. K., Baldwin, M. K., Tavares, L., Kaas, J. H.,  New Oligocene primate from Saudi Arabia and the di- & Herculano-Houzel, S. (address same as above). Brain, vergence of apes and Old World monkeys. Zalmout, I. S., Behavior and Evolution, 2010, 76, 45-59. Sanders, W. J., MacLatchy, L. M., Gunnell, G. F., Al- “The spinal cord can be considered a major sensorimo- Mufarreh, Y. A., Ali, M. A., Nasser, A.-A. H., Al-Masari, tor interface between the body and the brain. How does A. M., Al-Sobhi, S. A., Nadhra, A. O., Matari, A. H., Wil- the spinal cord scale with body and brain mass, and how son, J. A., & Gingerich, P. D. (Museum of Paleontology, are its numbers of neurons related to the number of neu- Univ. of Michigan, 1109 Geddes Ave, Ann Arbor, MI rons in the brain across species of different body and brain 48109 [e-mail: [email protected]]). Nature, 2010, 466, sizes? Here we determine the cellular composition of the 360-364, . ber of neurons varies as a linear function of cord length, “It is widely understood that Hominoidea (apes and and accompanies body mass raised to an exponent close to humans) and Cercopithecoidea (Old World monkeys) have

28 Laboratory Primate Newsletter, 2011, 50[1]

a common ancestry as Catarrhini deeply rooted in Afro- recently evolved, and combine avid inhibitory receptors Arabia. The oldest stem Catarrhini in the fossil record are with attenuated activating receptors. These differences Propliopithecoidea, known from the late Eocene to early accompany human-specific evolution of the A and B haplo- Oligocene epochs (roughly 35–30 Myr ago) of Egypt, types that are under balancing selection and differentially Oman and possibly Angola. Genome-based estimates for function in defense and reproduction. Our study shows divergence of hominoids and cercopithecoids range into how the qualitative differences that distinguish the human the early Oligocene; however, the mid-to-late Oligocene and chimpanzee systems of KIR and MHC class I pre- interval from 30 to 23 Myr ago has yielded little fossil evi- dominantly derive from adaptations on the human line in dence documenting the morphology of the last common response to selective pressures placed on human NK cells ancestor of hominoids and cercopithecoids, the timing of by the competing needs of defense and reproduction.” their divergence, or the relationship of early stem and  Endocranial shape changes during growth in chimpan- crown catarrhines. Here we describe the partial cranium of zees and humans: A morphometric analysis of unique and a new medium-sized (about 15–20 kg) fossil catarrhine, shared aspects. Neubauer, S., Gunz, P., & Hublin, J.-J. Saadanius hijazensis, dated to 29–28 Myr ago. Compara- (P.G., Dept of Human Evol., Max Planck Inst. for Evolu- tive anatomy and cladistic analysis shows that Saadanius is tionary Anthropology, Deutscher Platz 6, D-04103, an advanced stem catarrhine close to the base of the homi- Leipzig, Germany [e-mail: [email protected]]). noid–cercopithecoid clade. Saadanius is important for Journal of Human Evolution, 2010, 59, 555-566, assessing competing hypotheses about the ancestral mor- < photype for crown catarrhines, early catarrhine phylogeny linkinghub.elsevier.com/retrieve/pii/ and the age of hominoid–cercopithecoid divergence. S0047248410001442>. Saadanius has a tubular ectotympanic but lacks synapo- “Compared to our closest living and extinct relatives, morphies of either group of crown Catarrhini, and we infer humans have a large, specialized, and complex brain em- that the hominoid–cercopithecoid split happened later, be- bedded in a uniquely shaped braincase. Here, we quantita- tween 29–28 and 24 Myr ago.” tively compare endocranial shape changes during ontogeny in humans and chimpanzees. Identifying shared and  Human-specific evolution and adaptation led to major unique aspects in developmental patterns of these two spe- qualitative differences in the variable receptors of human cies can help us to understand brain evolution in the and chimpanzee natural killer cells. Abi-Rached, L., hominin lineage. Using CT scans of 58 humans and 60 Moesta, A. K., Rajalingam, R., Guethlein, L. A., & Par- chimpanzees varying in age from birth to adulthood, we ham, P. (P. P., Dept of Structural Biol., Stanford Univ. generated virtual endocasts to measure and analyze 29 Sch. of Med., Stanford, CA 94305-5101 [e-mail: three-dimensional endocranial landmarks and several hun- [email protected]]). PLoS Genetics, 2010, 6[11], dred semilandmarks on curves and the endocranial surface; . ric methods. The ontogenetic shape trajectories are “Natural killer (NK) cells serve essential functions in nonlinear for both species, which indicates several devel- immunity and reproduction. Diversifying these functions opmental phases. Endocranial shape is already distinct at within individuals and populations are rapidly-evolving birth and there is no overlap between the two species interactions between highly polymorphic major histocom- throughout ontogeny. While some aspects of the pattern of patibility complex (MHC) class I ligands and variable NK endocranial shape change are shared between humans and cell receptors. Specific to simian primates is the family of chimpanzees, the shape trajectories differ substantially Killer cell Immunoglobulin-like Receptors (KIR), which directly after birth until the eruption of the deciduous den- recognize MHC class I and associate with a range of hu- tition: in humans but not in chimpanzees, the parietal and man diseases. Because KIR have considerable species- cerebellar regions expand relatively (contributing to neuro- specificity and are lacking from common animal models, cranial globularity) and the cranial base flexes within the we performed extensive comparison of the systems of KIR first postnatal year when brain growth rates are high. We and MHC class I interaction in humans and chimpanzees. show that the shape changes associated with this early Although of similar complexity, they differ in genomic ‘globularization phase’ are unique to humans and do not organization, gene content, and diversification mecha- occur in chimpanzees before or after birth.” nisms, mainly because of human-specific specialization in  Brain development after birth differs between the KIR that recognizes the C1 and C2 epitopes of MHC-B Neanderthals and modern humans. Gunz, P., and -C. Humans uniquely focused KIR recognition on Neubauer, S., Maureille, B., & Hublin, J.-J. (Address same MHC-C, while losing C1-bearing MHC-B. Reversing this as above). Current Biology, 2010, 20, R921-R922, trend, C1-bearing HLA-B46 was recently driven to un- < precedented high frequency in Southeast Asia. Chimpan- download.cell.com/current-biology/pdf/ zees have a variety of ancient, avid, and predominantly PIIS0960982210012820.pdf>. inhibitory receptors, whereas human receptors are fewer, “Neanderthals had brain sizes comparable to modern humans, but their brain cases were elongated and not

29 Laboratory Primate Newsletter, 2011, 50[1]

globular as in Homo sapiens. It has, therefore, been sug- determine the source of variation in the composition of the gested that modern humans and Neanderthals reached large microbiota within and among species, we investigated the brain sizes along different evolutionary pathways. Here, distal gut microbial communities harbored by great apes, we assess when during development these adult differences as present in fecal samples recovered within their native emerge. This is critical for understanding whether differ- ranges. We found that the branching order of host-species ences in the pattern of brain development might underlie phylogenies based on the composition of these microbial potential cognitive differences between these two closely communities is completely congruent with the known rela- related groups. Previous comparisons of Neanderthal and tionships of the hosts. Although the gut is initially and modern human cranial development have shown that many continuously seeded by bacteria that are acquired from morphological characteristics separating these two groups external sources, we establish that over evolutionary time- are already established at the time of birth, and that the scales, the composition of the gut microbiota among great subsequent developmental patterns of the face are similar, ape species is phylogenetically conserved and has diverged though not identical. Here, we show that a globularization in a manner consistent with vertical inheritance.” phase seen in the neurocranial development of modern humans after birth is absent from Neanderthals.”  First skull of Antillothrix bernensis, an extinct relict monkey from the Dominican Republic. Rosenberger, A.  Radiometric dating of the type-site for Homo heidelber- L., Cooke, S. B., Rimoli, R., Ni, X., & Cardoso, L. (Dept gensis at Mauer, Germany. Wagner, G. A., Krbetschek, of Anthro. & Archaeol., Brooklyn Coll., CUNY, New M., Degering, D., Bahain, J.-J., Shao, O., Falguéres, C., York, NY [e-mail: [email protected]]). Proceed- Voinchet, P., Dolo, J.-M., Garcia, T., & Rightmire, G. P. ings of the Royal Society, B, 2011, 278, 67-74, (Geographisches Inst., Univ. Heidelberg, D-69120 Heidel- . ceedings of the National Academy of Sciences, U.S.A., The nearly pristine remains of Antillothrix bernensis, a 2010, 107, 19726-19730, . minican Republic, have been found submerged in an un- “The Mauer mandible, holotype of Homo heidelber- derwater cave. This represents the first specimen of an gensis, was found in 1907 in fluvial sands deposited by the extinct Caribbean primate with diagnostic craniodental and Neckar River 10 km southeast of Heidelberg, Germany. skeletal parts in association, only the second example of a The fossil is an important key to understanding early hu- skull from the region, and one of the most complete speci- man occupation of Europe north of the Alps. Given the mens of a fossil platyrrhine cranium yet discovered. Cra- associated mammal fauna and the geological context, the nially, it closely resembles living cebines but is more con- find layer has been placed in the early Middle Pleistocene, servative. Dentally, it is less bunodont and more primitive but confirmatory chronometric evidence has hitherto been than Cebus, with crowns resembling Saimiri (squirrel missing. Here we show that two independent techniques, monkeys) and one of the oldest definitive cebines, the late the combined electron spin resonance/U-series method Early Miocene Killikaike blakei from Argentina. The tri- used with mammal teeth and infrared radiofluorescence cuspid second molar also resembles the enigmatic marmo- applied to sand grains, date the type-site of Homo heidel- sets and tamarins, whose origins continue to present a ma- bergensis at Mauer to 609 ± 40 ka. This result demon- jor gap in knowledge of primate evolution. While the fe- strates that the mandible is the oldest hominin fossil re- mur is oddly short and stout, the ulna, though more robust, ported to date from central and northern Europe and raises compares well with Cebus. As a member of the cebid questions concerning the phyletic relationship of Homo clade, Antillothrix demonstrates that insular Caribbean heidelbergensis to more ancient populations documented monkeys are not monophyletically related and may not be from southern Europe and in Africa. We address the the product of a single colonizing event. Antillothrix paleoanthropological significance of the Mauer jaw in light bernensis is an intriguing mosaic whose primitive charac- of this dating evidence.” ters are consistent with an early origin, possibly antedating  Evolutionary relationships of wild hominids recapitu- the assembly of the modern primate fauna in greater Ama- lated by gut microbial communities. Ochman, H., zonia during the La Venta horizon. While most Greater Worobey, M., Kuo, C.-H., Ndjango, J.-B. N., Peeters, M., Antillean primate specimens are quite young geologically, Hahn, B. H., & Hugenholtz, P. (Dept of Ecology & Evolu- this vanished radiation, known from Cuba (Paralouatta) tionary Biol., Yale Univ., West Haven, CT 06520 [e-mail: and Jamaica (Xenothrix) as well as Hispaniola, appears to [email protected]]). PLoS Biology, 2010, 8[11], be composed of long-lived lineages like several other .  Chronology of the Grotte du Renne (France) and implica- “Multiple factors over the lifetime of an individual, tions for the context of ornaments and human remains including diet, geography, and physiologic state, will influ- within the Châtelperronian. Higham, T., Jacobi, R., Julien, ence the microbial communities within the primate gut. To M., David, F., Basell, L., Wood, R., Davies, W., & Ram-

30 Laboratory Primate Newsletter, 2011, 50[1]

sey, C. B. (Res. Lab. for Archaeology & History of Art, laboratory animals from June 1, 2008 to May 31, 2009. A Univ. of Oxford, Oxford OX1 3QY, U.K. [e-mail: thomas total of 11,337,334 live laboratory animals were being [email protected]]). Proceedings of the National maintained on June 1, 2009 in Japan. 11,416 (.1%) were Academy of Sciences, U.S.A., 2010, 107, 20234-20239, nonhuman primates. < >. www.pnas.org/content/107/47/20234.full Instruments and Techniques There is extensive debate concerning the cognitive and behavioral adaptation of Neanderthals, especially in the  Hypnotic effects and pharmacokinetics of a single bolus period when the earliest anatomically modern humans dis- dose of propofol in Japanese macaques (Macaca fsucata persed into Western Europe, around 35,000–40,000 B.P. fsucata). Miyabe-Nishiwaki, T., Masui, K., Kaneko, A., The site of the Grotte du Renne (at Arcy-sur-Cure) is of Nishiwaki, K., Shimbo, E., & Kanazawa, H. (K. M., Dept great importance because it provides the most persuasive of Anaesthesiology, Natl Defense Med. College, Namiki 3- evidence for behavioral complexity among Neanderthals. 2, Tokorozawa, Saitama, 359-8513 Japan. [e-mail: ken- A range of ornaments and tools usually associated with [email protected]]). Veterinary Anaesthesia and Analge- modern human industries, such as the Aurignacian, were sia, 2010, 37, 501-510, . site, along with Neanderthal fossil remains (mainly teeth). “Four male macaques (5–6 years old, 8.0–11.2 kg), This extremely rare occurrence has been taken to suggest were restrained and 8 mg/kg of propofol was administered that Neanderthals were the creators of these items. intravenously at 6 mg/kg/minute. Behavioral changes Whether Neanderthals independently achieved this level of without stimuli (first experiment), then responses to exter- behavioral complexity and whether this was culturally nal stimuli (second experiment) were assessed every 2 transmitted or mimicked via incoming modern humans has minutes for 20 minutes. Venous blood samples were col- been contentious. At the heart of this discussion lies an lected before and at 1, 5, 15, 30, 60, 120 and 210 minutes assumption regarding the integrity of the excavated re- after drug administration, and plasma concentrations of mains. One means of testing this is by radiocarbon dating; propofol were measured (third experiment). Pharmacoki- however, until recently, our ability to generate both accu- netic modelling was performed using NONMEM VI. The rate and precise results for this period has been compro- macaques were recumbent without voluntary movement mised. A series of 31 accelerator mass spectrometry ul- for a mean 14.0 ± 2.7 SD (range 10.5–16.2) or 10.0 ± 3.4 trafiltered dates on bones, antlers, artifacts, and teeth from (7.2–14.5) minutes and recovered to behave as pre- six key archaeological levels shows an unexpected degree administration by 25.1 ± 3.6 (22.1–30.1) or 22.2 ± 1.5 of variation. This suggests that some mixing of material (21.1–24.3) minutes after the end of propofol administra- may have occurred, which implies a more complex deposi- tion without or with stimuli, respectively. Respiratory and tional history at the site and makes it difficult to be confi- heart rates were stable throughout the experiments (28–68 dent about the association of artifacts with human remains breaths/minute and 72–144 beats/minute, respectively). in the Châtelperronian levels. Our final pharmacokinetic model included three compart- General ments and well described the plasma concentration of propofol. The population pharmacokinetic parameters were:  Survey of live laboratory animals reared in Japan (2009). V1 = 10.4 L, V2 = 8.38 L, V3 = 72.7 L, CL1 = 0.442 Yagami, K., Mashimo, T., Sekiguchi, F., Sugiyama, F., L/minute, CL2 = 1.14 L/minute, CL3 = 0.313 L/minute, Yamamura, K., & Serikawa, T. (LARC, Univ. of Tsu- (the volumes of distribution and the clearances for the cen- kuba, 1-1-1 Tennodai, Tsukuba, Ibaraki 305-8575, Ja- tral, rapid and slow peripheral compartments, respec- pan). Experimental Animals, 2010, 59, 531-535, tively). We conclude that intravenous administration of . caques had a hypnotic effect lasting more than 7 minutes. A survey on the number of live laboratory animals A three-compartment model described propofol plasma reared in research institutions, including universities, bio- concentrations over more than 3 hours. The developed medical institutes, testing laboratories, pharmaceutical pharmacokinetic parameters may enable simulations of companies, and animal breeders, was conducted on June 1, administration protocols to maintain adequate plasma con- 2009. One thousand seventy-four replies were recovered centration of propofol.” from 1,593 institutions, and 471 of them had used live * * *

CONTENTS

Articles and Notes Dead Infant Carrying in the Hanuman Langur (Semnopithecus entellus) Around Jodhpur (Rajasthan), by G. Sharma, B. Swami, C. Ram, & L. S. Rajpurohit...... 1 Rita the Chimpanzee (Pan troglodytes ellioti): The Start of an Enrichment Program at the Doha Zoo, Qatar, by H. Tresz...... 5 Separating Cage-Mates Temporarily – A LAREF Discussion ...... 10 News, Information, and Announcements Meeting Announcements ...... 11 Information Requested or Available...... 11 Great Apes in Japan; New ASP Website; More Interesting Websites Resources Available ...... 12 Special OLAW Online Seminar; CANTAB Cognitive Testing System; 2011 Bonobo Calendar; Hominoid Carrying Archive Online; Procedures with Care; Lincoln Park Zoo’s Blood Type Database for Apes Resources Wanted: Videos of the Birthing Process ...... 13 ASLAP Veterinary Student Award Program...... 13 Research and Educational Opportunities...... 14 Veterinary Residency, New York; Laboratory Animal Science Management Courses; Wildlife Studies and Primatology – Japan; Education and Training in Field Primatology; Husbandry for Zoo and Aquarium Animals – Mexico News Briefs...... 15 Devra G. Kleiman: Conservation Biologist; Will Aging Research Chimpanzees Be Relocated? NY Must Release Records on Monkey Research; AVMA Revises Veterinarian’s Oath; Gorilla Tested for Possible Human Disease; Census: Mountain Gorilla Population Grows President Obama Honors Nation’s Top Scientists and Innovators...... 17 Announcements from Publications: The Journal of Evolutionary Biology Research ...... 17 Departments Recent Books and Articles...... 18